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Departments of Animal Sciences and * Basic Medical Sciences, Purdue University, West Lafayette, IN 47907
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: • ducks • ontogeny • intestine • hydrolase • L-threonine
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). This was attributed in
part to meat-type animals having a larger gastrointestinal tract
relative to body mass, consuming threefold more food and possessing
two- to fivefold higher disaccharidase activities. Low-molecular-weight
nutrients, including free amino acids, are transported into the
enterocytes of the small intestine by brush border membrane-bound
transport systems. The capacity of the intestinal mucosa to transport
free amino acids from the gut lumen dictates the ability of an animal
to attain conditions of optimal protein accretion. The ontogeny of
intestinal brush border hydrolases (Biviano et al. 1993
,
Ferraris et al. 1992
, Matasushita 1985
)
and intestinal brush border amino acid transport systems
(Buddington and Diamond 1990
, Hayashi and Kawasaki 1982
, Obst and Diamond 1992
,
Soriano and Planas 1998
, Tolza and Diamond 1992
) have been studied extensively in several vertebrate
species. These studies have reported age-related differences in
small intestine hydrolase activities and amino acid transport rates and
have also suggested that intestinal amino acid uptake capacities were
closely matched to intakes of the adults in some species. However,
investigations of the developmental patterns of digestive functions of
avian species other than the domesticated chicken are not well
documented. The purpose of this study was to investigate the developmental patterns of two small intestine brush border hydrolases (sucrase and alkaline phosphatase) and L-threonine transport system(s) in male White Pekin ducks (Maple Leaf commercial strain). In addition, several intestinal tissue characteristics were measured, including intestinal weight, length, and nominal surface area and mucosal weight. This study related changes in intestinal tissue measurements, intestinal hydrolase activity and intestinal brush border L-threonine transport capacity to the duck’s biological development.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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3H-L-Threonine was obtained from Amersham (Arlington Heights, IL). Ecolume scintillant was obtained from IGN (Costa Mesa, CA). Bio-Rad dye reagent for protein determination was purchased from Bio-Rad Laboratories (Richmond, CA). Bovine serum albumin (fraction V), L-threonine, D-mannitol, Trizma-HCl, HEPES, phenylmethylsulfonyl fluoride (PMSF)3 and other chemicals were purchased from Sigma Chemical (St. Louis, MO).
Preparation of mucosal scrapings.
In the experiment, 50 1-d-old male White Pekin ducklings (Anas
platyhrynchos), provided by Maple Leaf Farms (Syracuse, IN)
were housed in cages equipped with feeders and waterers. Temperature in
the room was controlled by ventilation fans and thermostatically
controlled. Fluorescent bulbs provided light for 24 h. Ducklings
had free access to water and the same feed for 7 wk. The analyzed diet
contained 230 g/kg crude protein, 14.3 g/kg lysine, 7.7 g/kg methionine
+ cysteine, 9.3 g/kg threonine and 13.30 MJ nitrogen-corrected
apparent metabolizable energy (AMEn)/kg. The
AMEn of the diet was determined as previously described
(Adeola et al. 1997
). Ducks were weighed at wk 1, 3, 5
and 7. Eight to twenty ducks, depending on the age of the ducks, were
randomly selected at wk 1 (n = 20), wk 3
(n = 12), wk 5 (n = 10) and wk
7 (n = 8) and their intestines harvested.
For the isolation of the small intestinal segments, ducks were killed by decapitation (1 and 3 wk) or by intravenous injections of Beuthanasia (0.25 mL/kg, Schering-Pough Animal Health, Kenilworth NJ). The small intestines were excised and rinsed with ice-cold solution (154 mmol/L NaCl, 0.1 mmol/L PMSF, Trizma-HCl, pH 7.4). The intestines were opened longitudinally and freed of mucus by patting with paper towel. The intestinal mucosa were removed by scraping the luminal surface firmly with glass slides. Because very little mucosa was obtained from 1- and 3-wk-old birds, mucosa for hydrolase and amino acid transport assays were pooled from five and three ducks, respectively. Mucosa from the older groups were collected and stored for individual ducks. The total small intestine weights, mucosa weights, lengths and nominal surface areas (minus amplification by villi and microvilli; length x width of longitudinally opened intestine) of the intestines were measured for the different age groups. The Purdue University Animal Care and Use Committee approved the experimental protocol.
Protein and hydrolase assays.
Protein was determined colorimetrically with a DU-640 spectrophotometer
at 595 nm (Beckman Instruments, Fullerton, CA) according to the method
of Bradford (1976)
. Sucrase (EC 3.2.1.48) was assayed
according to the procedure of Dahlqvist (1964)
. The
intestinal mucosal homogenate or brush border membrane vesicles were
incubated with sucrase at 40°C, and the liberated glucose was
measured by a glucose-specific hexokinase reaction.
Alkaline phosphatase (orthophosphoric monoester phosphohydrolase, EC
3.1.3.1) was assayed according to Engstrom (1964)
. The intestinal mucosal homogenate or brush
border membrane vesicles were incubated with
p-nitrophenyl phosphate at 40°C. Alkaline phosphatase
(ALP) hydrolyzes p-nitrophenyl phosphate to
p-nitrophenol and inorganic phosphate.
Enzyme activities were normalized to protein content. Total intestinal
hydrolase activities (µmol hydrolyzed/min) over the
entire intestine were estimated as specific enzyme activity in mucosal
homogenate x homogenate protein content per gram mucosa x total mucosa weight (Zhang et al. 1997
).
Preparation of brush border membrane vesicles.
The brush border membrane vesicles (BBMV) were prepared according to
the modified Mg2+-precipitation procedure for chickens
(Maenz and Engele-Schaan 1996
). The resultant crude
BBMV suspensions were transferred to cryogenic vials in 2-mL aliquots
(Nalgen Company, Rochester, NY) and frozen in liquid nitrogen until
use. For a given uptake experiment, a suitable number of aliquots of
BBMV suspensions were thawed in 50 mL of vesicle resuspension buffer
(150 mmol/L D-mannitol, 200 mmol/L KSCN, 50 mmol/L HEPES,
pH 7.4, adjusted with Trizma-base). The resuspended crude vesicles were
then homogenized in a prechilled glass Wheaton tissue grinder (Wheaton,
Millville, NJ) with 8 strokes before centrifugation at 30,100 x g for 45 min to generate the brush border membrane
pellets. The pellets were resuspended with a 26-gauge needle, in a
suitable volume of vesicle resuspension buffer (150 mmol/L
D-mannitol, 200 mmol/L KSCN, 50 mmol/L HEPES, pH 7.4
adjusted with Trizma-base) to give the final brush border membrane
vesicle suspension. This suspension was then assayed for protein
content and diluted with the resuspension buffer to give a BBMV
suspension that contained 15 g protein/L for uptake measurements.
Amino acid transport assay.
L-Threonine uptake experiments were conducted with a rapid
filtration technique (Fan et al. 1998
). Threonine is one
of the essential amino acids in poultry nutrition and is often the
third limiting amino acid when avian species are fed diets based on
corn and soybean meal (Leclercq 1998
). Three uptake
experiments were conducted for each age group with brush border
membrane vesicle suspensions prepared from intestinal mucosal scrapings
of ducks. A time period of 5 s was used to measure the initial
rate of threonine transport under Na+-gradient condition.
Total L-threonine uptake capacity (µmol/s)
was calculated as follows: maximum L-threonine flux
(Jmax) x total brush border membrane
vesicle protein x brush border membrane protein recovery factor.
Brush border membrane protein recovery factor was calculated as
follows: total mucosal protein sucrase activity/total brush border
membrane sucrase activity. Daily L-threonine uptake
capacity was calculated as follows: total threonine uptake capacity
x 86,400, where 86,400 is the number of seconds in a day. Daily
feed intakes were estimated following the procedure of
Buddington and Diamond (1990)
. Estimates of normal
threonine intakes were based on ducks consuming 11.64, 11.60, 8.49 and
7.19% of their body weights daily at 1, 3, 5 and 7 wk, respectively
(NRC 1994
).
Statistics.
Statistical analyses were performed with the SAS software (SAS Institute 1995
) using the General Linear Models procedure.
Values in the text are presented as means ± SEM.
Means were separated with least significant difference at a
significance level of P < 0.05. The kinetic
parameters were estimated from the Eadie-Hofstee transformation of
the transport-mediated component of the total substrate uptake.
Linear regression analyses were conducted with the FigP software (FigP, 1993, Biosoft, Cambrige, UK).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Ducks increased > ninefold in body weight from 1 wk posthatch to
7 wk posthatch (Table 1
). For the age range studied, intestinal weight, surface area and length
relative to body weight were maximal at 1 wk. Relative growth rates
were fastest during wk 1 posthatch and then declined through to wk 7 of
life, with a threefold increase in body weight from wk 1 to 3 and less
dramatic increases thereafter. The fresh weight of the small intestine
increased threefold from 1 wk posthatch to age 7 wk. The ratio of
intestinal surface area (cm2) to body weights (g)
decreased from 1:2 at age 1 wk to 1:5, 1:6 and 1:7 at wk 3, 5 and 7,
respectively. The intestinal weights as a percentage of body weights
declined as the ducks aged.
|
). Metabolic live weight is defined as the body
weight0.75 because the metabolic rates of
vertebrates are related to body weights0.75.
Therefore, intestinal weight was directly proportional to metabolic
live weight. When the log surface area was plotted against log body
weight, the slope was 0.54 ± 0.08. This slope was lower than the
coefficient for metabolic weight.
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The protein concentration of the mucosa homogenates remained relatively
constant and ranged from 103 to 129 mg protein/g mucosa (Table 2
). Although sucrase activity was present at 1 wk, homogenate specific
activity was low and relatively constant from 1 to 5 wk. There was then
an immoderate increase (P < 0.05) in sucrase specific
activity at 7 wk. Homogenate ALP specific activity did not change from
1 to 7 wk (P > 0.05). Total hydrolytic activity was
highest (P < 0.05) at 7 wk for sucrase and constant
(P > 0.05) for ALP for the age groups studied. Total
homogenate sucrase activity per gram mucosa and per unit area
(cm2) increased at 7 wk (P < 0.05). Total homogenate ALP activity per gram mucosa and per unit area
(cm2) remained relatively constant from 1 to 7 wk
(P > 0.05). Total homogenate sucrase activity/100 g
body weight did not differ among the age groups studied (P
> 0.05). Total homogenate ALP activity/100 g body weight
decreased (P < 0.05) at 3 wk and then remained
relatively constant from 3 to 7 wk (P > 0.05).
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The initial L-threonine uptake rates were highest
(P < 0.05) at 3 wk and were 43, 56 and 66% higher
than those of the 1-, 5- and 7 wk-old groups, respectively
(Table 3). The Michaelis constants for the transporter
(Kt) were 600, 300, 350 and 370
µmol/L for the 1-, 3-, 5- and 7-wk-old ducks,
respectively. The plot of log estimated L-threonine uptake
capacity against log body weight had a slope that was lower than the
coefficient for metabolic live weight (Fig. 1)
. The estimated
L-threonine uptake capacity normalized to body weight was
highest (P < 0.05) at 1 wk and then gradually declined
to its lowest levels at 7 wk. The ratios of daily
L-threonine intake to estimated uptake capacities indicated
that estimated daily L-threonine intakes were considerably
higher than daily uptakes at 5 and 7 wk.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, Matasushita 1985
, Obst and Diamond 1992
, Planas et al. 1986
, Shehata et al. 1981
, Soriano and Planas 1998
), each with
differing focuses on solutes, intestinal regions and age range studied.
Other domesticated avian species have not received equivalent
attention. The duck is an excellent model for ontogenetic studies of
intestinal enzymes and nutrient transporter systems because this
species is rapidly growing and precocial. Therefore, by feeding
ducklings a diet of constant composition while they are being raised,
food intake rates are determined by the ducklings rather than by the
parents. Hence, the confounding effects of different diets fed to each
age group, as is often the case with mammalian ontogenetic studies, are
avoided, and changes in hydrolase and amino acid uptake rates can be
attributed to ontogenetic development programs. Furthermore, in this
study, intestinal brush border L-threonine uptake ontogeny
was examined in terms of the duck’s biology and nutritional
requirements, which is more useful from a practical standpoint than
simply characterizing L-threonine transport across small
intestinal brush border membrane vesicles of ducks at a specific age.
In White Pekin ducks, intestinal growth was in direct proportion to the
age-related increases in metabolic rates. In addition, as the ducks
grew, intestinal tissues became a smaller proportion of total body
tissues. The tissue quantity changes in the chicken small intestine
during development reported by Soriano et al. (1993)
paralleled those found in this study, in which intestinal weight,
surface area and length relative to body weight were maximal during wk
1 of life and declined rapidly as the chickens aged. In this and other
studies done on avian species, the allometric growth coefficients
(Japanese quail, 0.61; turkey, 0.69; chickens 0.74) appear to be
indistinguishable from metabolic rate coefficients (Lilja 1983
, Obst and Diamond 1992
). It appears that
the intestines of avian species grow in direct proportion to the
age-related increases in metabolic rates. Furthermore, in avian
species, patterns of intestinal growth appear to be correlated with
patterns of whole-body growth rates. For this reason, some
researchers have proposed that whole-body growth rates are
determined in part by the allocation of tissue to the gastrointestinal
tract (Konarzewski et al. 1989
, Lilja 1983
, Obst and Diamond 1992
). The results from
this study support the premise that rapid intestinal hyperplasia is a
prerequisite for sustained rapid posthatch growth in avian species.
The results from this study indicated that ducks have the ability to
digest sucrose early in their lives. In chickens, intestinal mucosa
sucrase activity was detected at 10 d of incubation and reached
adult levels 3 d after hatching (Matasushita 1985
).
A dramatic increase in glucose transport was reported 2 wk posthatch in
chickens (Obst and Diamond 1992
), coinciding presumably
with two physiologic events, i.e., yolk sac depletion and the
acquisition of thermal and locomotory independence. If a corresponding
peak in glucose occurred in ducks in the first few weeks posthatch,
then sucrase activity would also be expected to increase during this
period. No sucrase peak was detected in this study. Because no samples
were taken between d 7 and 21 and between d 21 and 35, it cannot be
concluded categorically that a peak in sucrase catalytic activity did
not occur during this period. However, sucrose is not an important part
of the diets of granivorous birds; hence, ontogenetic changes in
sucrase activity may not be important to these species because the
majority of their carbohydrate intake is consumed in the form of starch
and amylopectin (Biviano et al. 1993
). Earlier workers
have indicated that several digestive tract–associated enzymes in
birds show changes in molecular species during ontogeny (Yasugi et al. 1979
, Yasugi and Mizuno 1981
). The
significant increase in sucrase at 7 wk in this study may be the result
of changes in the sucrase isozyme patterns.
No significant increase in ALP activity was found in this study in duck
intestinal mucosa for the age groups investigated. Palo et al. (1995)
reported a peak in broiler chicken ALP activity at 2 wk
that appears to correspond to the yolk sac depletion and the
achievement of locomotory independence in chickens during this period.
In this study, however, the developmental course of total ALP
hydrolytic capacities normalized to body mass paralleled the course of
relative body growth rates. This pattern correlates well with the
results of previous works that indicated that ducks require less
phosphorus and other minerals per gram body weight as they age
(Scott and Dean 1991
). In mammals, the
intestinal ALP has been suggested to be the same enzyme as the phytase
enzyme (Yang et al. 1991
). Phytate forms complexes with
proteins as well or mono- and divalent cations and is estimated to
account for 50–80% of the total phosphorus content of legumes and
grains (Sandberg et al. 1993
). Some studies have
reported that chickens can retain up to 60% of dietary phytate
phosphate (Edwards 1983
, Temperton and Cassidy 1964a
and 1964b
). Thus, phytate phosphorus is an important
source of phosphorus for granivorous birds.
In this study, initial L-threonine uptake rates were
highest at 3 wk. These results are comparable to those reported in
chickens (Buddington and Diamond 1989
, Obst and Diamond 1992
); in that species, peaks for the initial uptake
rates of essential amino acids and glucose occurred in wk 2 and 3
posthatch. In contrast, Gonzalez and Vinardell (1996)
used an in vivo method to study the ontogenic development of proline
transport in domestic fowl and found no spike in transport during the
first weeks posthatch. They speculated that this might be possible
because of the way the data in the in vivo experiment were expressed
compared with those of Diamond et al. (1986)
. Diamond
and co-workers presented their results as dry or fresh weight,
whereas Gonzalez and Vinardell (1996)
standardized their
results to surface area. Moreover, the increased uptake rates observed
with brush border techniques may be counterbalanced by a concomitant
increase in the basolateral efflux permeability when whole tissues are
used in nutrient transport experiments (Ferrer et al. 1994
). The developmental course of L-threonine
uptake capacity normalized to body mass observed in White Pekin ducks
from 1 to 7 wk showed a decline with age that appeared to parallel
relative growth rates. This trend is consistent with the development of
digestive functions in several species in which functions related to
protein assimilation declined with age (Buddington and Diamond 1989
). Soriano and Planas (1998)
found a similar
trend in small intestine capacities of 1- to 13-wk-old male White
Leghorns to transport L-proline. These results agree with
earlier reports in the literature that indicated absolute increases in
uptake capacities; however, concurrent declines in uptake capacities
normalized to body weight occurred as vertebrates aged
(Buddington and Diamond 1989
).
No differences were observed in either Jmax
or Kt under Na+-gradient
conditions during development for the age groups of White Pekin ducks
examined in this study. A report by Hayashi and Kawasaki (1982)
indicated a developmental decrease in the
Kt and no change in the
Jmax for proline uptake by guinea pig ileal
brush border membrane vesicles. Apparent
Jmax values of 71 pmol/(mg protein·s) and
Kt values of 0.8 mmol/L were calculated for
Na+-dependent transport of glutamine into porcine jejunal
brush border vesicles (Fan et al. 1998
). Methionine
uptake into chicken intestinal brush border membranes under conditions
of an inwardly directed Na+-gradient had apparent
Jmax and Kt
values of 554 pmol/(mg protein·s) and 0.14 mmol/L, respectively
(Maenz and Engele-Schaan 1996
). These results and
the data from this study suggest that amino acid kinetic parameters are
similar for avian species but differ between avian and other species.
Alterations in nutrient uptake rates during ontogenic development are
subjected to many factors including the modification in membrane
surface area, shifts in membrane lipid to protein ratios, cell
metabolism and the density of transport systems per square centimeter
of intestine (Shehata et al. 1981
).
In the in vitro experiment, uptake to intake ratios were well below 1
for the 5- and 7-wk-old ducks. However, the amino acid uptake assay was
conducted at room temperature, whereas the normal body temperature of
ducks is 41°C. Hence, L-threonine uptake capacities are
likely to be higher in vivo. Furthermore, in this study, the
solvent-drag component of nutrient uptake was assumed to be
insignificant under physiologic conditions. Although
Pappenheimer and Reiss (1987)
have contended that
paracellular intestinal nutrient transport by solvent-drag accounts
for most nutrient uptake in vivo, their calculations were based on
erroneously high luminal nutrient concentrations documented in early
studies. It was previously believed that transport capacities of adult
vertebrates greatly exceeded dietary inputs. Recent studies that used
physiologic nutrient concentrations, however, have indicated that
transport capacities generally exceeded estimates of intakes by less
than an order of magnitude (Buddington and Diamond 1989
). The question of "digestive bottlenecks" in
vertebrates, i.e., that the uptake capacity of the intestine to
assimilate nutrients poses a proximal constraint on rate of growth, has
been addressed by Diamond and co-workers for a number of species
(Buddington and Diamond 1990
and 1992
, Diamond et al. 1986
, Obst and Diamond 1992
, Tolza and Diamond 1992
). Indeed, digestive bottlenecks have been
reported in several adult species, including ruminants and hummingbirds
(Diamond et al. 1986
, Krebs and Harvey 1986
), whereas several other species appear to have large
uptake relative to intake capacities. In general the uptake/intake
ratios of rats and rabbits reported were generally several fold higher
than that of chickens (Buddington and Diamond 1990
,
Tolza and Diamond 1992
). In chickens, amino acid ratios
of intestinal uptake capacity to dietary intake are ~1.0 (Obst and Diamond 1992
), indicating that growing chickens may
function close to their assimilation summit. The data from this study
also indicate that growing White Pekin ducks may function near their
assimilation summit. The successive decrease in the
L-threonine ratios of intestinal uptake capacity to dietary
intake corresponded to the decline in relative body growth rates that
were observed in ducks in this study. If this is true for other
essential nutrients, relative increases in body weights of ducks may be
confined by the limitations of nutrient uptake by the gut, with a
consequential deprivation of nutrients to tissues undergoing rapid
hyperplasia.
The critical period in duckling nutrition appears to be from hatching to 3 wk posthatch. Therefore, extreme vigilance should be given to the duck’s nutrition during this period in which essential amino acid uptake to intake capacity ratios appear to be maximal. The results presented are from a fast-growing White Pekin duck strain, and similar intestinal changes may not occur in other rapidly growing breeds and strains of ducks. Comparable to the relationship between ingestion and uptake of nutrients, the relationships between hydrolase digestion and nutrient uptake capacities should be examined in a quantitative fashion. When such information is applied to feed formulation, ducklings could be fed more adequately, according to their biological development and changing posthatch nutritional needs.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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3 Abbreviations used: ALP, alkaline phosphatase;
AMEn, nitrogen-corrected apparent metabolizable energy;
BBMV, brush border membrane vesicles; Jmax,
maximum L-threonine flux; Kt,
Michaelis constant for the transporter; PMSF,
phenylmethylsulfonylfluoride; WB, body
weight; WI, intestinal weight.
Manuscript received June 23, 1999. Initial review completed July 29, 1999. Revision accepted September 23, 1999.
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