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Sex-Dependent Dysregulation of Human Neutrophil Responses by Bisphenol A

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Sex-Dependent Dysregulation of Human Neutrophil Responses by Bisphenol A Ratajczak-Wrona et al. Environmental Health (2021) 20:5 https://doi.org/10.1186/s12940-020-00686-8 RESEARCH Open Access Sex-dependent dysregulation of human neutrophil responses by bisphenol A Wioletta Ratajczak-Wrona1* , Marzena Garley1 , Malgorzata Rusak2 , Karolina Nowak1 , Jan Czerniecki3 , Katarzyna Wolosewicz1 , Milena Dabrowska2 , Slawomir Wolczynski3,4 , Piotr Radziwon5 and Ewa Jablonska1 Abstract Background: In the present study, we aimed to investigate selected functions of human neutrophils exposed to bisphenol A (BPA) under in vitro conditions. As BPA is classified among xenoestrogens, we compared its action and effects with those of 17β-estradiol (E2). Methods: Chemotaxis of neutrophils was examined using the Boyden chamber. Their phagocytosis and nicotinamide adenine dinucleotide phosphate hydrogen (NADPH) oxidase activity were assessed via Park’s method with latex beads and Park’s test with nitroblue tetrazolium. To assess the total concentration of nitric oxide (NO), the Griess reaction was utilized. Flow cytometry was used to assess the expression of cluster of differentiation (CD) antigens. The formation of neutrophil extracellular traps (NETs) was analyzed using a microscope (IN Cell Analyzer 2200 system). Expression of the investigated proteins was determined using Western blot. Results: The analysis of results obtained for both sexes demonstrated that after exposure to BPA, the chemotactic capacity of neutrophils was reduced. In the presence of BPA, the phagocytic activity was found to be elevated in the cells obtained from women and reduced in the cells from men. Following exposure to BPA, the percentage of neutrophils with CD14 and CD284 (TLR4) expression, as well as the percentage of cells forming NETs, was increased in the cells from both sexes. The stimulatory role of BPA and E2 in the activation of NADPH oxidase was observed only in female cells. On the other hand, no influence of E2 on the expression of CD14 and CD284, chemotaxis, phagocytosis, and the amount of NET-positive neutrophils was found for both sexes. The study further showed that BPA intensified NO production and iNOS expression in the cells of both sexes. In addition, intensified expression of all tested PI3K-Akt pathway proteins was observed in male neutrophils. Conclusions: The study demonstrated the influence of BPA on neutrophil functions associated with locomotion and pathogen elimination, which in turn may disturb the immune response of these cells in both women and men. Analysis of the obtained data showed that the effect of this xenoestrogen on the human neutrophils was more pronounced than E2. Keywords: Neutrophils, Bisphenol A, 17β-estadiol, Nitric oxide * Correspondence: [email protected] 1Department of Immunology, Medical University of Bialystok, ul. Waszyngtona 15A, 15-269 Bialystok, Poland Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Ratajczak-Wrona et al. Environmental Health (2021) 20:5 Page 2 of 18 Background everyday products, such as food storage containers and The primary cell components of the innate immune fluids, plastic bottles, and infant feeding bottles. The system are phagocytes, which include neutrophils. They human exposure to the compound occurs mainly via the perform a wide spectrum of functions and thus consti- oral route due to the fact that the BPA particles that tute the first line of defense against pathogenic microor- were not polymerized completely during the production ganisms and neoplastic cells. In addition, neutrophils process are released from packaging to foods. BPA is serve as regulatory and effector cells in the mechanisms also absorbed via the skin by contact with the thermal of the acquired immune response. The neutrophils paper used to print receipts (e.g. ATM receipts) [25–28]. present in the bloodstream are metabolically inactive It has also been demonstrated to be present in many tissues and do not exhibit cytotoxic properties [1–6]. On receiv- and fluids including whole blood, umbilical cord blood, and ing a chemical signal, the cells are stimulated and move urine [26, 29, 30]. An analysis conducted by the National to the site of infection/inflammation (chemotaxis). On Health and Nutrition Examination Survey showed the pres- their surface, neutrophils possess receptors that can ence of BPA at a concentration of 1.8–660 nM in urine recognize the molecular patterns of pathogens (PRMs) samples in the majority of US residents [31, 32]. and can therefore identify foreign particles and differen- BPA is a xenoestrogen—a chemical compound that tiate them from their own. The PRMs include, inter alia, resembles steroid hormones in its structure. It is classi- Toll-like receptors (e.g. TLR4), the ligand for which is fied among the endocrine-disrupting compounds (EDC) lipopolysaccharide—LPS [1, 5, 7, 8]. One of the strat- or endocrine disruptors. EDCs constitute a group of egies used by neutrophils to kill pathogens is phagocyt- chemical compounds produced by people and do not osis, which involves the stages such as “recognition” and occur naturally in the environment. These compounds “absorption” of the pathogen and formation of a phago- modulate the intrasecretory activity by affecting the lysosome. Inside the phagolysosome, the absorbed biosynthesis, metabolism, and hormone actions. The pathogen is killed by any of the two mechanisms: aerobic toxicity of these compounds cannot be accurately deter- (associated with the production of reactive oxygen spe- mined. The dosage and effect of EDCs seem to exhibit cies (ROS) and reactive nitrogen species) and anaerobic nonmonotonic relationships; both extremely low and (associated with the presence of proteins contained in high dosages can provide a maximum response, while the granules) [7, 9–13]. Another strategy used by neu- the medium doses are associated with the concomitant trophils as the first line of defense to fight against patho- absence of effect. This dosage–effect response of EDCs genic microorganisms is the creation of neutrophil is often presented as a U-shaped curve, or also in the extracellular traps—NETs. This phenomenon involves form of an inverted U-shaped curve, where medium the release of the cellular nucleus contents (decondensed dosing provides the maximum effect [33–38]. chromatin and histone proteins) together with the com- Data show that BPA may affect the signaling pathways ponents of granularity (including myeloperoxidase associated with the nuclear (estrogen receptor (ER)-α (MPO)) and cell cytoplasm into the extracellular space. and ERβ) and membrane receptors (GPR30) of estrogens In addition to neutralizing and destroying the pathogens, [39]. Research studies indicate that the nuclear receptors NETs prevent their proliferation by creating a physical are present in both female and male neutrophils [40]. barrier [10, 14–20]. It is hypothesized that neutrophils In light of the current knowledge, it is assumed that hu- prefer fast phagocytosis when they come in contact with man neutrophils are also the target cells of BPA. However, small microorganisms, whereas when recognizing larger the molecular mechanisms of the action of this xenobiotic pathogens or aggregates of microorganisms, they activate on neutrophils are not fully characterized. Earlier works the NET formation [21]. have shown the effect of BPA on neutrophil immunophe- One of the reactive nitrogen radicals produced by the notypes as well as its gender-dependent effects on the activated neutrophils is nitric oxide (NO). It is produced intracellular killing of neutrophils associated with the re- with the action of nitric oxide (NO) synthase enzymes, lease of serine proteases [41, 42]. Therefore, we conducted which include inducible nitric oxide synthase (iNOS), further studies in women and men to find answers to the through the oxidation of L-arginine. The expression and following questions: Can BPA affect the basic neutrophil activity of iNOS can be controlled by both endogenous functions? If so, does this effect depend on gender? To and exogenous factors [22, 23]. Previous studies have better understand the basis of the molecular action mech- demonstrated that bisphenol A (BPA) affects the pro- anism of this xenobiotic on the functions of the studied duction of NO by human neutrophils, with differences leukocyte population, especially those related to NO syn- in the activity of NF-κB transcription factor in neutro- thesis and release, we assessed the
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