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Alteration of Prostaglandin Production and Agonist Responsiveness by N-6 Polyunsaturated Fatty Acids in Endometrial Cells from Late-Gestation Ewes

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Alteration of Prostaglandin Production and Agonist Responsiveness by N-6 Polyunsaturated Fatty Acids in Endometrial Cells from Late-Gestation Ewes 249 Alteration of prostaglandin production and agonist responsiveness by n-6 polyunsaturated fatty acids in endometrial cells from late-gestation ewes Z Cheng, M Elmes, S E Kirkup,DREAbayasekara and D C Wathes Reproduction and Development Group, Royal Veterinary College, Hawkshead Lane, North Mymms, Hatfield, Herts AL9 7TA, UK (Requests for offprints should be addressed to D C Wathes; Email [email protected]) Abstract We investigated the effect of n-6 polyunsaturated fatty alterations in responsiveness as a result of PUFA treatment. acids (PUFAs) on prostaglandin (PG) production by In the cells supplemented with 100 µM AA, there was no the uterus. A mixed population of endometrial cells further increase in PGF2 output in the presence of OT or (epthelium and stroma) from late-gestation ewes were LPS and when 100 µM GLA was present neither LPS nor cultured in defined medium containing linoleic acid OT stimulated PGE2 significantly. When LPS was given (LA, 18:2, n-6), -linolenic acid (GLA, 18:3, n-6) or to AA-supplemented cells, the E:F ratio was increased. arachidonic acid (AA, 20:4, n-6) in concentrations of 0 DEX did not change PGE2 production in control or (control), 20 or 100 µM. After 45 h in test medium with or LA-treated cells, but the cells produced significantly less without added PUFAs, cells were challenged with control PGF2, so the E:F ratio was increased. In contrast, in medium (CM), oxytocin (OT, 250 nM), lipopolysaccha- GLA- and AA-treated cells, DEX reduced the production ride (LPS, 0·1 µg/ml) or dexamethasone (DEX, 5 µM) for of both PGF2 and PGE2, so the E:F ratio was unaltered. 22 h in the continued presence of the same concentration In summary, the study showed altered production of PGs of PUFA and the medium was collected for measurement in the presence of different PUFAs according to their of PGF2 and PGE2. Supplementation with LA inhibited position in the n-6 metabolic pathway. The type of PUFA ff the production of PGF2 but did not alter PGE2, whereas present a ected responsiveness to OT, LPS and DEX and GLA and AA increased production of both PGs. All PUFA also changed the ratio of PGE2 to PGF2 produced. supplements thus increased the ratio of PGE2 to PGF2 The possible implications of this work are discussed in (E:F ratio) two- to threefold. In control cells, OT and relation to the effect of diet on term and pre-term labour, LPS challenges stimulated the production of PGF2 and which both require upregulation of the endometrial PG PGE2. In all challenge groups, the concentrations of synthetic pathway. PGF2 in response to PUFAs followed the same pattern – Journal of Endocrinology (2004) 182, 249–256 LA<control<GLA<AA – but there were significant Introduction as the precursors for a variety of signalling molecules and influence many fundamental cell processes. LA is an Cardiovascular disease is the principal cause of death essential fatty acid, which is metabolised in the body to among the human population of developed countries, with GLA, dihomo--linolenic acid (DGLA, 20:3, n-6) and the saturated fat content of the diet identified as one of arachidonic acid (AA, 20:4, n-6) by the position-specific the major risk factors (Department of Health 1995). This 6 and 5 desaturase and coenzyme A (CoA)-dependent finding has promoted a trend to reduce dietary intakes of chain elongases (Sprecher 2000). Cyclo-oxygenases meat and dairy products in favour of a substantial increase (COX) catalyse conversion of DGLA and AA into 1- and in vegetable oils, which are high in n-6 polyunsaturated 2-series prostaglandins (PGs) respectively. fatty acids (PUFAs), notably linoleic acid (LA, 18:2, n-6). In the n-6 PUFA metabolic pathway from LA to AA, Oils containing -linolenic acid (GLA, 18:3, n-6), such as there are two rate-limiting catalytic steps, 6 and 5 primrose oil, are also promoted as health products, because desaturases. The amount of LA converted to GLA is tiny of their potential anti-inflammatory and anti-proliferative and only a small fraction of GLA can be catalysed into AA properties (Fan & Chapkin 1998). Dietary PUFAs provide (Fan & Chapkin 1998). Supplementation with GLA energy and components for cell membranes. They also act bypasses the rate-limiting 6 desaturase and GLA is Journal of Endocrinology (2004) 182, 249–256 Online version via http://www.endocrinology.org 0022–0795/04/0182–249 2004 Society for Endocrinology Printed in Great Britain Downloaded from Bioscientifica.com at 09/28/2021 09:25:41PM via free access 250 Z CHENG and others · Effects of PUFAs on endometrial PG production quickly elongated to DGLA by elongase. DGLA can in several agonists known to play an important part in natural turn be converted into 1-series PGs, such as PGF1 and or pre-term labour were also examined by testing the PGE1. Supplementation with AA avoids the limitation of responsiveness of the cells to OT, LPS and DEX. 5 desaturase and AA is directly converted to 2-series PGs, such as PGF2 and PGE2, by COX enzymes (Lapetina 1982). This suggests that supplementary PUFAs Materials and Methods may alter the n-6 PUFA metabolic pathway and that the precise effects of PUFAs on PG production will depend on All reagents were from Sigma (Poole, Dorset, UK) or their position in the pathway. BDH Merck Ltd (Lutterworth, Leics, UK) unless other- Considerable attention has been paid to the effects of wise stated. Solutions were sterilised by passage through a PUFA supplementation on carcinogenesis, because PGs 0·20 µm filter (Nalge Nunc International, Rochester, NY, have an important role in the regulation of tumour growth USA or Millipore Company, Bedford, MA, USA). All (Bishop-Bailey et al. 2002, Dommels et al. 2002). To date, culture media used included 50 000 units/l penicillin and relatively little information is available about the possible 50 mg/l streptomycin. effects of increased n-6 PUFA concentrations on the production of PG in relation to reproductive processes Cell isolation and culture (Abayasekara & Wathes 1999). Previous studies have produced contradictory results, in that feeding dairy cows Gravid uteri were obtained on day 135 of gestation (term a diet high in LA caused either a decreased (Thatcher et al. is approximately 145 days). Ewes were killed using an 1994, Cheng et al. 2001a) or an increased (Robinson overdose of pentabarbitone and the reproductive tract was et al. 2002) production of 2-series PG by the uterine collected. endometrium. Graham et al. (1994) found a reduced Endometrial cells were isolated and cultured under ability of the endometrium to produce PGF2 and PGE2 sterile conditions in a laminar flow hood, following in women who had been taking a dietary supplement of methods described previously (Cheng et al. 2003). From GLA for 6 months. the intercotyledonary region of the uterus, maternal Upregulation of the 2-series PGs, in particular PGE2 endometrium was separated, cut into strips and put into and PGF2, is an essential component of parturition serum-free Dulbecco’s minimal essential medium/F12 1:1 (Challis 2000). In the ewe, activation of the fetal nutrient mix (DMEM/F12 medium, Gibco Life hypothalamic–pituitary–adrenal axis in late gestation leads Technologies, Paisley, Strathclyde, UK) containing to increased production of PGE2 by the placenta and 1·125 g/l fatty-acid-free bovine serum albumin (BSA, subsequent initiation of parturition (Thorburn 1991). In Sigma) and 1·125 g/l sodium bicarbonate at pH 7·3. The phase 1 of labour, the increased cortisol output stimulates strips were then chopped into 1 mm3 cubes using the conversion of androgen to oestrogen in the placenta, a McIlwain mechanical tissue chopper (McIlwain upregulates the expression of COX-2 and downregulates Laboratory Engineering, Guilford, Surry, UK). Two the production of PG dehydrogenase (PGDH), resulting in aliquots of 20 g chopped tissue were placed into two falcon increased production of PGE2 (Challis et al. 2002). In vials and mixed with 30 ml digestive solution. This phase 2 of labour, oxytocin (OT) receptors are upregulated contained 0·05% trypsin III (Roche, Diagnostic GmbH, in the intercotyledonary endometrium (Leung et al. 1999) Mannheim, Germany), 0·05% collagenase II (Roche) and and mediate increased release of PGF2 in response to 0·1% BSA (Sigma) in Hank’s Balanced Saline (HBS, OT (Jenkin 1992), resulting in uterine contractions and Sigma). After incubation for 2 h at 37 C with shaking, delivery (Whittle et al. 2001, Challis et al. 2002). Synthetic the suspensions were filtered through a 100 µm mesh. glucocorticoids such as dexamethesone (DEX) can mimic The filtrates were pooled into a 50 ml falcon vial and the endogenous increase in cortisol and induce parturition re-suspended with washing medium [HBS containing (Challis et al. 2002). Pregnant women given exogenous 10% (v/v) fetal calf serum (FCS, Sigma) and 3 µg/ml corticosteroids to promote fetal maturation have an trypsin inhibitor (Sigma)]. The vial was then centrifuged at increased incidence of pre-term birth (Challis et al. 2002). 100 g and 4 C for 10 min. The supernatant was removed Intrauterine infection is another major risk factor in and the pellet re-suspended with washing medium. After pre-term labour (Goncalves et al. 2002). The bacterial two repetitions of the above washing procedures, the cell endotoxin, lipopolysaccharide (LPS), increased the pellets containing mixed epithelial and stromal cells were activities of phospholipase (PL) A2 and COX-2 and re-suspended in DMEM/F12 medium containing 10% inhibited PGDH (Lamont et al. 1990, Flynn & Hoff 1995, FCS to a concentration of 0·5106 cells/ml. This cell van Meir et al.
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