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Metabolism and Transport of Maternal Serine by the Ovine Placenta: Glycine Production and Absence of Serine Transport Into the Fetus

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Metabolism and Transport of Maternal Serine by the Ovine Placenta: Glycine Production and Absence of Serine Transport Into the Fetus 003 1-3998/93/3306-0590$03.00/0 PEDIATRIC RESEARCH Vol. 33, No. 6, 1993 Copyright 0 1993 International Pediatric Research Foundation, Inc. Printed In U.S. A. Metabolism and Transport of Maternal Serine by the Ovine Placenta: Glycine Production and Absence of Serine Transport into the Fetus RUSSELL R. MOORES, JR., CHRISTINE C. TH. RIETBERG, FREDERICK C. BATTAGLIA, PAUL V. FENNESSEY, AND GIACOMO MESCHIA Division of Perinatal Medicine, Departments of Pharmacology, Physiology, and Pediatrics, University of Colorado School of Medicine, Denver, Colorado 80262 ABSTRACT. The present study compares the transplacen- (3). On the other hand, there is a large umbilical uptake of tal transport of L-[1-I3C]serineand L-[l-13C]leucinein sheep. glycine (4) without measurable uterine uptake of glycine (2, 5, An in vivo preparation using twin gestations was set up 6). However, the absence of a measurable net uterine uptake of such that the arterial circulation to one uterine horn, glycine is not convincing due to the high uterine blood flow of including its placenta and fetus, was infused with tracer pregnancy and maternal plasma glycine concentration. Even a serine and leucine while the umbilical circulations of both 2% coefficient of extraction across the uterine circulation, which fetuses were sampled. Uterine and umbilical blood flows would not be easy to detect, would represent an appreciable were measured in each horn. Plasma serine enrichments uterine uptake of glycine. These data suggest the possibility that were 14.6 f 2.7% and 4.3 f 1.6% in the uterine veins serine derived from the maternal plasma pool may be used within draining the experimental and control horns, respectively. the placenta for glycine production and that this may contribute Fetal plasma leucine enrichments in the umbilical veins substantially to the glycine supply to the fetus from the placenta. were 50 and 55% of the uterine venous enrichments in the Recent studies in our laboratory using tracer serine infusion into control and experimental fetuses, respectively. By contrast, the fetal circulation have shown that in both late gestation (7) during 280 min of infusion, there was no detectable serine and midgestation (8), fetal plasma serine is utilized within the enrichment in either fetal circulation. However, significant placenta for glycine production. plasma glycine enrichment was present in the fetal circu- The present study was designed to test the hypothesis that lation of the experimental horn and venous glycine enrich- maternal serine contributes to the fetal amino acid pool primarily ments in the experimental horn were significantly greater through serine to glycine conversion in the uteroplacental tissues. than arterial glycine enrichments for both the umbilical (p This study uses a new stable isotope infusion technique in twin < 0.02) and uterine (p < 0.001) circulations. We conclude pregnancies such that the uteroplacenta of one twin is selectively that under conditions in which leucine transport is easily exposed to high [ I -I3C]serine and [ 1 -13C]leucineconcentrations demonstrable there is no significant transplacental trans- via the maternal circulation while the appearance of leucine, port of maternal serine and that maternal plasma serine is serine, and glycine in the fetal circulation of both twins is used within the uteroplacental tissues for producing gly- monitored. Leucine transport and metabolism have been well cine, some of which is delivered into the fetal circulation. described in late gestation ovine pregnancy (9-1 1) and thus can (Pediatr Res 33: 590-594, 1993) serve as a useful reference point in interpreting the transfer of other amino acids. The animal model used in these studies uses Abbreviations one uterine horn and its fetus as a control in that glycine production from serine in maternal tissues such as the maternal SHMT, serine hydroxymethyltransferase liver will be presented with equal enrichment to both uterine horns, whereas serine enrichment will be higher in the arterial blood perfusing the infused, experimental horn. By this ap- proach, uteroplacental glycine production from serine can be distinguished from glycine production elsewhere in the maternal The fetal protein accretion associated with fetal growth re- organism. quires that at least the essential amino acids be transported across the placenta into the umbilical circulation. In contrast, the fetal demand for the nonessential amino acids may be met by any MATERIALS AND METHODS combination of placental transport and/or synthesis within the Biologic preparation. Three pregnant twin gestation Columbia- fetus and placenta. In adult metabolism, it has been clearly Rambouillet ewes were studied at approximately 126 d gestation demonstrated that there is organ-specific production and utili- (term = 147 d). After an overnight fast, surgery was performed zation of serine and glycine (I). Studies of the net uterine and under pentobarbital sedation and spinal anesthesia with tetra- fetal uptakes of glycine and serine in ovine pregnancy have caine. The preparation developed was such that the placenta of yielded somewhat confusing results. On the one hand, a net one twin (experimental fetus) could be exposed selectively to a uterine uptake of serine from the maternal circulation has been high concentration of tracer through local uterine artery infusion found (2) without any net flux of serine into the fetal circulation (Fig. 1). Polyvinyl catheters used for sampling the fetal circulation Received November 23, 1992; accepted February 4, 1993. were placed into the common umbilical vein and an external Correspondence and reprint requests: Frederick C. Battaglia, M.D., University iliac artery of each fetus. Catheters were also placed into a fetal of Colorado School of Medicine, Department of Pediatrics, Division of Perinatal brachial vein for infusion of blood flow indicators into each fetus Research, 4200 East Ninth Ave., Box B-199, Denver, CO 80262. Supported by NIH Program Project Grant HD-00781 and NIH Grant HD- (3H20,ethanol and/or antipyrine). Previous studies have shown 01866. no significant differences among these indicators for measure- 5 SERINE PLACENTAL TRANSPORT AND METABOLISM 59 1 MATERNAL SYSTEMIC CIRCULATION Each catheter was irrigated daily with heparinized saline. An intraamniotic injection of 500 mg of ampicillin was administered daily for 3 d after surgery. Experimental protocol. The studies were performed 3 to 5 d after surgery when the animals were fully recovered and eating normally. Studies were performed with the animals conscious and allowed full access to food and water. An infusate consisting of 750 mg of L-[l-'3C]serine and 500 mg of L-[l-13C]leucinewas prepared in 100 mL of sterile saline solution. This solution was infused into the uterine artery catheter for approximately 5 h resulting in infusion rates of 5.2 and 3.3 pmol/min for labeled serine and leucine, respectively. Two solutions, each containing one of the flow indicators, were prepared in sterile saline for determination of uterine and umbilical blood flows in each uterine horn and its fetus. These solutions were infused simul- taneously into the experimental and control fetuses at a constant rate for the duration of the study. With this model, the concen- trations of [l-'3C]serine and [I-'3C]leucine reaching the placenta of the experimental twin through the local uterine artery infusion would be significantly greater than that reaching the placenta of the control twin, because in the latter case it is diluted by the maternal amino acid pool. At the same time, uterine and umbil- ical blood flows could be separately determined in each uterine horn. Before the start of the infusion, time zero samples were ob- tained from each catheter. After allowing 170 to 180 min for the Fig. 1. Scheme of the experimental preparation that selectively ex- attainment of a steady state, five sets of blood samples were poses the placenta of one twin fetus (experimental placenta) to a high drawn simultaneously from each catheter at approximately 25- concentration of tracer serine and leucine. min intervals. After completion of the experiment, each ewe was given a Table 1. Fetal age, fetal weight, umbilical bloodyow, uterine rapid i.v. infusion of euthanasia solution. At autopsy, the weights bloodflow, and fetal oxygen consumption* of each fetus and placenta were obtained, and the positions of the catheters were confirmed. Experimental Control Chemical analysis. Blood samples for blood gas analysis were Fetal age (d) 126 a 3 126 t 3 collected in glass capillary tubes lined with dried heparin. Hb Fetal wt (kg) 2.31 + 0.1 2.35 + 0.1 concentration expressed as oxygen capacity and oxygen satura- Umbilical blood flow (mL. 244 + 14 219 t 24 tion was measured with a Radiometer (Copenhagen, Denmark) min-I. kg fetus-') hemoximeter. Oxygen content was calculated as the product of Uterine blood flow (mL.min-I) 70 1 + 142 700 + 130 the Hb and the oxygen saturation. Fetal oxygen consumption 344 + 26 408 + 46 Blood for mass svectral isotove ratio analysis, amino acid (fimol. min-I. kg fetus-') analysis, ethanol, 3H20,and antipyrine concentrations were coi- *Values are means + SEM. In each case, n = 3. lected in plastic syringes lined with dried EDTA. Ethanol (l3), 3H20(14), and antipyrine (15) concentrations were determined ments of umbilical blood flow (12). Catheters for sampling the as previously described. Plasma for amino acid and mass spectral maternal circulation were inserted into both uterine veins (ex- analysis was immediately stored at -70°C. perimental and control horns) and one maternal femoral artery. Amino acid concentrations were determined as previously A catheter for infusion of the I3C-labeled amino acids was reported using a JEOL-200A amino acid analyzer (JEOL USA, inserted and advanced 1 cm downstream into a branch of the Cranford, NJ) with norleucine as the internal standard (1 6). The uterine artery supplying blood to the placenta of only one fetus. mass spectral isotope ratio analysis of serine, glycine, and leucine Amniotic catheters were inserted for antibiotic administration.
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