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Composition and Permeability of Syncytiotrophoblast Plasma Membranes in Pregnancies Complicated by Intrauterine Growth Restriction

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Composition and Permeability of Syncytiotrophoblast Plasma Membranes in Pregnancies Complicated by Intrauterine Growth Restriction View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Biochimica et Biophysica Acta 1420 (1999) 86^94 www.elsevier.com/locate/bba Composition and permeability of syncytiotrophoblast plasma membranes in pregnancies complicated by intrauterine growth restriction Theresa L. Powell a;*, Thomas Jansson a, Nicholas P. Illsley b, Margareta Wennergren c, Marina Korotkova d, Birgitta Strandvik d a Perinatal Center, Department of Physiology and Pharmacology, Go«teborg University, Box 432, S-405 30 Go«teborg, Sweden b Department of Obstetrics and Gynecology, UMDNJ-New Jersey Medical School, Newark, NJ, USA c Department of Obstetrics and Gynecology, Sahlgrenska University Hospital, Go«teborg University, Go«teborg, Sweden d Department of Pediatrics, Sahlgrenska University Hospital, Go«teborg University, Go«teborg, Sweden Received 9 March 1999; received in revised form 18 May 1999; accepted 27 May 1999 Abstract The objective of this study was to determine placental membrane permeabilities to water, urea and mannitol in intrauterine growth restriction (IUGR) and compare them to normal gestational age matched controls. Further, we wished to investigate whether potential changes in permeability were related to changes in membrane fluidity, cholesterol or phospholipid fatty acid content of the membranes. Syncytiotrophoblast microvillous (MVM) and basal membranes (BM) were isolated from normal and IUGR placentas at term. Passive permeability to water, urea, and mannitol showed no significant alterations in IUGR compared to controls. Cholesterol content in BM, but not in MVM, was lower in placentas from pregnancies complicated by IUGR. However, membrane fluidity did not change in these pregnancies. The phospholipid fatty acid composition of the plasma membranes isolated from all placentas showed a predominance of unsaturated fatty acid species in the BM and saturated species in the MVM. In the MVM from IUGR, mead acid (20:3), behenic acid (22:0) and nervonic acid (24:1) constituted higher percentages of the total when compared to normally grown controls. In the BM from IUGR, mead acid (20:3) was increased relative to the total phospholipid fatty acid content. In conclusion, the syncytiotrophoblast membranes exhibit only minor changes in passive permeability and composition when the pregnancy is complicated by IUGR. ß 1999 Elsevier Science B.V. All rights reserved. Keywords: Placenta; Membrane; Permeability; Human; Essential fatty acid; Intrauterine growth restriction 1. Introduction tal transport in the human. There are two possible pathways for solutes to permeate the syncytiotropho- Normal fetal growth and development is depend- blast layer: a transcellular route requiring permea- ent on su¤cient transport of nutrients from the ma- tion of both the microvillous and basal plasma mem- ternal to fetal circulation. The syncytiotrophoblast branes or through water ¢lled trans-trophoblastic layer constitutes the primary barrier for transplacen- channels. It has been assumed that hydrophilic mol- ecules are transported across the placenta almost ex- clusively by means of water ¢lled channels [1]. Per- * Corresponding author. Fax: +46-31-773-3512; meabilities to hydrophilic molecules of the term E-mail: [email protected] human placenta have been studied in vivo [2^5] 0005-2736 / 99 / $ ^ see front matter ß 1999 Elsevier Science B.V. All rights reserved. PII: S0005-2736(99)00096-6 BBAMEM 77648 3-8-99 T.L. Powell et al. / Biochimica et Biophysica Acta 1420 (1999) 86^94 87 and using in vitro perfused tissue [6,7]. Syncytiotro- with low birth weight [23]. Other studies have shown phoblast plasma membranes isolated from term pla- that an altered placental fatty acid composition may centa have also been used to de¢ne the permeabilities be related to IUGR [24], pre-eclampsia [25] and pre- of these plasma membranes to a range of non-elec- term labor [26]. However, the phospholipid fatty acid trolyte solutes [8] and water [9]. The data from iso- composition of the isolated syncytiotrophoblast plas- lated plasma membranes suggest that a transcellular ma membranes has not been previously reported. route may account for a signi¢cant portion of the in Changes in EGA, LCPUFA or cholesterol content vivo permeability for small hydrophilic solutes in the in these membranes would a¡ect the £uidity as well human placenta [8]. as the passive permeation of important fetal nu- Alterations in plasma membrane composition af- trients. We tested the hypothesis that pregnancies fect membrane order, £uidity and lipid-protein inter- complicated by IUGR have an altered syncytiotro- actions. A number of studies have shown that the phoblast plasma membrane permeability and compo- activity of membrane bound enzymes and passive sition. permeability to small solutes are altered with changes in membrane composition due to dietary in£uences [10^12]. Likewise, clinical conditions such as cystic 2. Materials and methods ¢brosis [13,14], diabetes [15^17], cigarette smoking and alcohol consumption [18] are associated with 2.1. Membrane isolation and characterization alterations in membrane fatty acid composition, per- meability and enzymatic activity. Altered placental In order to study placental transcellular permeabil- membrane lipid composition in pregnancy would af- ity and determine the lipid composition of the syn- fect transcellular transport but not permeation cytiotrophoblast plasma membranes, we simultane- through water ¢lled channels. Assuming that the ously isolated microvillous (MVM) and basal (BM) transcellular component is a signi¢cant proportion membranes from human placentas obtained from of total transport of biologically important substan- pregnancies complicated by IUGR and from healthy, ces such as water, glucose and amino acids, then gestational age matched controls. Human placental alterations in membrane composition and passive tissue was obtained immediately following delivery permeability might be involved in a variety of preg- and processed according to protocols approved by nancy complications. Passive permeability character- the local ethical committee for Go«teborg University istics of the human placenta in abnormal pregnancies and Sahlgrenska University Hospital, Go«teborg, are largely unknown. Sweden. Selected clinical characteristics for the pa- Pregnancies complicated by intrauterine growth re- tient population from which placentas were obtained striction (IUGR) are those in which the fetus fails to are given in Table 1. IUGR was de¢ned as a birth reach its genetic growth potential. A current theory weight two standard deviations below the population based on epidemiological data suggests that maternal mean for gestational age and sex. The normal term nutritional state may play an important role in this group included only uncomplicated pregnancies. condition and that adult health may be predeter- MVM and BM were prepared simultaneously from mined by fetal nutritional status in utero [19]. Devel- placentas as described previously [27]. Approxi- oping fetuses are dependent on the placenta for mately 100 g of villous tissue was dissected away transport of essential fatty acids (EFA) and their from the chorionic plate, decidua and fetal mem- derivatives, long chain polyunsaturated fatty acids branes. The tissue was washed in bu¡ered saline (LCPUFA). These fatty acids are major components and homogenized (at 4³C, in bu¡er D: 250 mM su- of cellular membranes, precursors to eicosanoids and crose, 10 mM HEPES-Tris pH 7.4, 1.6 WM antipain, are critical for organogenesis and proper growth. 0.7 WM pepstatin A, 0.5 WM aprotinin, 1 mM Developmental de¢ciencies in EFA have been linked EDTA). Di¡erential centrifugation steps were con- to neurological [20,21] and visual disorders [22]. Ma- ducted (two runs at 10 000Ug for 15 min followed ternal undernutrition a¡ects the free fatty acid com- by 125 000Ug for 30 min, at 4³C) to remove cellular position of placental homogenates and is correlated debris. From the crude membrane fraction the MVM BBAMEM 77648 3-8-99 88 T.L. Powell et al. / Biochimica et Biophysica Acta 1420 (1999) 86^94 Table 1 2.2. Permeability measurements Selected clinical data Normal term IUGR term All permeability measurements were performed at n 910 37³C using a Hi-Tech SF 51 stopped £ow apparatus Maternal age (years) 33.6 þ 1.5 31.9 þ 1.7 (Salisbury, Wiltshire, UK) with a 50 W quartz halo- Gestational age (weeks) 38.6 þ 0.4 38.1 þ 0.2 gen lamp in series with a single grating monochro- Smokers (n)12 mator (excitation 500 þ 5 nm) as a light source. Os- Route of delivery motic water permeability (Pf) was measured by vaginal 1 4 cesarean 8 6 subjecting membrane vesicles loaded with 150 mM Placental weight (g) 649 þ 46 405 þ 26* ra¤nose in 5 mM HEPES-Tris pH 7.4 to a 100 Birth weight (g) 3474 þ 117 2230 þ 73* mOsm/kg outwardly directed osmotic gradient. The Mean þ S.E.M. *P 6 0.05, Student's t-test. subsequent vesicle shrinkage was monitored (2500 data points per experiment) by measuring the inten- were separated by Mg2 precipitation and BM were sity of scattered light and single exponential curves further puri¢ed on a discontinuous sucrose step gra- were ¢tted to the experimental data. Pf was calcu- dient (140 000Ug for 60 min at 4³C). A ¢nal wash in lated by comparing single exponential time constants bu¡er D and centrifugation (125 000Ug for 30 min, to simulated curves as previously described [9]. Per- at 4³C) of both membrane samples was conducted. meabilities to urea and mannitol (Ps) were measured Samples were resuspended in bu¡er D and snap fro- using published protocols [29]. Brie£y, membrane zen in liquid nitrogen and stored at 380³C until use. vesicles were subjected to 100 mOsm/kg inwardly di- Using alkaline phosphatase activity [28] as a rected solute gradients under isoosmotic conditions. marker for MVM and forskolin (30 WM) stimulated Vesicle swelling, due to water entry following the adenylate cyclase activity as a BM marker, this prep- permeation of solute, was monitored by the decrease aration produced plasma membranes with a high in the intensity of scattered light.
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