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Association Between Increased Expression of Endothelial Isoform of Nitric Oxide Synthase in the Human Fallopian Tube and Tubal Ectopic Pregnancy

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Association Between Increased Expression of Endothelial Isoform of Nitric Oxide Synthase in the Human Fallopian Tube and Tubal Ectopic Pregnancy Iran J Reprod Med Vol. 12. No. 1. pp: 19-28, January 2014 Original article Association between increased expression of endothelial isoform of nitric oxide synthase in the human fallopian tube and tubal ectopic pregnancy Leyla Fath Bayati1 M.Sc., Marefat Ghaffari Novin1, 2 M.D., Ph.D., Fatemeh Fadaei Fathabadi1 Ph.D., Abbas Piryaei1 Ph.D., Mohammad Hasan Heidari1 Ph.D., Mozhgan Bandehpour2 Ph.D., Mohsen Norouzian1 Ph.D., Mahdi Alizadeh Parhizgar3 M.D., Mahmood Shakooriyan Fard3 B.Sc. 1. Department of Biology and Abstract Anatomical Sciences, Faculty of Medicine, Shahid Beheshti Background: Tubal ectopic pregnancy (tEP) is the most common type of extra- University of Medical Sciences, uterine pregnancy and the most common cause of maternal mortality. Nitric oxide Tehran, Iran. (NO) is a molecule that incorporates in many physiological processes of female 2. Cellular and Molecular Biology reproductive system. Recent studies have demonstrated the possible role of Research Center, Shahid Beheshti University of Medical endothelial isoform of nitric oxide synthase (eNOS) enzyme in the regulation of Sciences, Tehran, Iran. many reproductive events that occur in the fallopian tube (FT). 3. Department of Pathology, Objective: The aim of this study was to evaluate the expression of eNOS in the FTs Kamkar Arab-Niya Hospital, of women with tEP. Qom University of Medical Sciences, Qom, Iran. Materials and Methods: In this case-control study, a total number of 30FTs samples were obtained from three groups including: 10 FTs of women that bearing an EP, 10 FTs from the non-pregnant women at luteal phase of the menstrual cycle, and 10 FTs of healthy pregnant women (n=10). Samples were fixed in 10% buffered formalin and then were evaluated by immunohistochemistry. Results: Localization of eNOS was seen in secretory and ciliated luminal epithelium and vascular endothelium of all groups. However, we did not observed the expression of eNOS in smooth muscle cells of all groups. Expression of eNOS in luminal epithelium of women with EP compared to non-pregnant women at luteal Corresponding Author: phase of menstrual cycle and healthy pregnant group showed statistically significant Marefat Ghaffari Novin, Cellular increase (p=0.00). Significant difference in expression of eNOS was not observed in and Molecular Biology Research Center, Shahid Beheshti University luminal epithelium of FTs of women at luteal phase compared to healthy pregnant of Medical Sciences, Tehran, Iran. groups (p=0.78). PO. Box. 1985717443 Conclusion: This study indicates that changes in expression of eNOS in luminal Email: [email protected] epithelium of FT may lead to development of EP. Tel: (+98) 21 23872555 Received: 22 December 2012 Key words: Ectopic pregnancy, Nitric oxide, Immunohistochemistry, Fallopian tube. Revised: 1 June 2013 This article extracted from M.Sc. thesis. (Leyla Fath Bayati) Accepted: 21 September 2013 Introduction (1, 7-11). Maintaining of embryo within the fallopian tube as a result of improper transport ctopic pregnancy (EP), the and deleterious tubal alteration can lead to implantation of a fertilized ovum tubal ectopic pregnancy (tEP) (12). Successful E outside the endometrial lining of tubal transport of gametes and blastocyst is uterine cavity, accounts for leading cause of substantial for fertilization, early embryo morbidity and mortality in women development, and intrauterine pregnancy. reproductive-age (1-4). It accounts for 1.5-2% Effective transportation within the tube is of all pregnancies in the western world and obtained by interactions between muscle more than 95% of EP occurs in the fallopian contractions; ciliary beating and factors that tubes (FTs), mainly in the ampulla region (5, secreted by fallopian tube (13). 6). The etiological causes for EP include Ovarian hormones and other factors damage to the fallopian tube due to previous produced by the fallopian tube, such as tubal surgery, pelvic inflammatory disease, prostaglandins, Nitric oxide (NO), prostacyclin cigarette smoking, assisted reproductive and cAMP may also regulate muscle technology, endometriosis and history of EP contraction and play significant role in embryo Fath Bayati et al transport (14-21). Also, transport of embryo or tubal implantation of blastocyst and the within the fallopian tube is influenced by ciliary development of EP (13). As mentioned above, beats which is regulated by factors such as production of NO by the human fallopian tube sex steroid hormones and IL-6 (22-24). has been previously reported, and effect of Results of the previous studies demonstrated this messenger molecule on relaxation of that ovarian follicular fluid contains factors that tubal smooth muscle cells was documented could affect ciliary beating in the fallopian tube (17, 42, 43). Also, in a recent study, iNOS during ovulation period (25). mRNA and protein levels were shown to be Findings of previous study shown that NO greater in the fallopian tube of women with could affect the contraction of fallopian tube tEP compared with pseudo pregnant women smooth muscle and ciliary beat frequency in (44). epithelial cells of airway via cyclic guanosine In the present study, we investigated the mono phosphate (cGMP) pathway (17, 18, 26, expression of eNOS in different group, 27). Others reported that endothelin, a potent because eNOS is the main isoform of NOS contracting factor are produced by bovine expressed in the oviduct (27). Our study oviduct and is able to induce contraction of investigated that whether the fallopian tubes oviduct (28-30). They also demonstrated that bearing an EP differed from normal tubal the contractile properties of endothelin-1 on tissues in expression of eNOS. As mentioned bovine oviducts are enhanced by the in previous studies human Fallopian tube is presence of N-monomethyl-L-arginine mono the most frequent site for EP. We acetate (L-NMMA), an inhibitor of NO hypothesized that regulation of eNOS may be synthesis. These findings provided the first altered in the process of EP, and this can be indirect evidence for endogenous synthesis of considered as one of potential causes of NO within the oviduct (30). inability to successful pregnancy. NO is a free radical that is produced from L-arginine in the process of its conversion to Materials and methods L-citrullin by the action of nitric oxide synthase (NOS) enzyme, an enzyme existing in three All techniques, methods and selection of isoforms (31). Neuronal NOS (nNOS or patients were approved by ethical committee NOS1) and endothelial NOS (eNOS or of Shahid Beheshti University of Medical NOS3), also referred to as constitutive NOS Sciences. Tissue was obtained from patients (cNOS), are responsible for the continuous at Vali-e-asr and Izadi Hospitals in Qom, Iran. basal release of NO and both require calcium/ The patients were informed in detail about the calmodulin for activation (32, 33). Third study and written consent was obtained from isoform of NOS is an inducible calcium- each case. Time of sample collection lasted independent form (iNOS or NOS2) that is from August 2011 to March 2012. expressed only in response to inflammatory cytokines and lipopolysaccharides (LPS) (34, Sample collection and preparation of 35). The three isoforms of NOS are products sections of separate genes that share 50-60% amino In this case control study, immune acid homology (36). histochemical localization of eNOS were NO has different physiological activity, assessed in FTs of women in three groups including regulation of vascular resistance, including, FTs of women bearing an EP contribution in cellular injury, and signal (n=10), FTs of women in luteal phase of transduction (37-39). NO is a double-edged menstrual cycle (n=10) and FTs of healthy sword. At low concentration, it alters 2+ pregnant women (n=10). intracellular Ca levels and induces smooth muscle relaxation (40). But at high Case Group concentration, it can lead to immune reaction The ectopic pregnancy group (n=10) and tissue damage (41). NO has an important consisted of women (29.00±3.70 years, range role in smooth muscle relaxation and ciliary 24-35 and average estimated gestational age activity so has attracted many researches calculated from the last menstrual period focusing on these fields (38, 23). In fallopian (LMP) was 5.66±2.55 weeks: data shown at tube impaired ciliary beating and smooth mean±SE) that bearing an ectopic pregnancy. muscle cells contractions may lead to infertility Salpingectomy in this group was performed on 20 Iranian Journal of Reproductive Medicine Vol. 12. No. 1. pp: 19-28, January 2014 eNOS in the human Fallopian tube clinical management ground. All participants and distribution of eNOS immune staining conceived spontaneously and were not taking between three groups. A polyclonal rabbit exogenous progesterone. We excluded cases antihuman antibody was used to detect eNOS in which the EP was due to reflux after in vitro (ABcam Company, UK). Paraffin-embedded fertilization (IVF). Also we excluded the tubal tissue sections (3 μm) were women who were cigarette smoker or have deparaffinized in xylene and rehydrated in prior history of pelvic inflammatory disease ethanol series (100%, 96%, and 80%). (PID). Antigen retrieval was performed in a microwave in 10 mmol/L citric acid buffer, pH Control Group 6.0, for 14 minutes. The luteal phase group (n=10) consisted of Slides were allowed to be cool at room women that were at luteal phase of menstrual temperature and were washed three times in cycle (38.33 ± 6.63 years, range 28-49 years) PBS before being incubated with methanol- who presented for total abdominal H2O2 (96:4, v/v) for 15 minutes to inhibit hysterectomy (TAH) due to benign disease endogenous peroxidase. The slides were then that not affected the fallopian tubes. All exposed to1.5% normal gaot serum (DAKO women at luteal phase group who donated Co, Denmark) in humidified chambers for 30 FTs had regular menstrual cycles and we minutes at room temperature to avoid excluded the women that had evidence of unspecific bindings of antibody.
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