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      Bacterial lipopolysaccharide induces apoptosis in the trout ovary


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          In mammals it is well known that infections can lead to alterations in reproductive function. As part of the innate immune response, a number of cytokines and other immune factors is produced during bacterial infection or after treatment with lipopolysaccharide (LPS) and acts on the reproductive system. In fish, LPS can also induce an innate immune response but little is known about the activation of the immune system by LPS on reproduction in fish. Therefore, we conducted studies to examine the in vivo and in vitro effects of lipopolysaccharide (LPS) on the reproductive function of sexually mature female trout.


          In saline- and LPS -injected brook trout, we measured the concentration of plasma steroids as well as the in vitro steroidogenic response (testosterone and 17alpha-hydroxyprogesterone) of ovarian follicles to luteinizing hormone (LH), the ability of 17alpha,20beta-dihydroxy-4-pregnen-3-one to induce germinal vesicle breakdown (GVBD) in vitro, and that of epinephrine to stimulate follicular contraction in vitro. We also examined the direct effects of LPS in vitro on steroid production, GVBD and contraction in brook trout ovarian follicles. The incidence of apoptosis was evaluated by TUNEL analysis. Furthermore, we examined the gene expression pattern in the ovary of saline- and LPS-injected rainbow trout by microarray analysis.


          LPS treatment in vivo did not affect plasma testosterone concentration or the basal in vitro production of steroids, although a small but significant potentiation of the effects of LH on testosterone production in vitro was observed in ovarian follicles from LPS-treated fish. In addition, LPS increased the plasma concentration of cortisol. LPS treatment in vitro did not affect the basal or LH-stimulated steroid production in brook trout ovarian follicles. In addition, we did not observe any effects of LPS in vivo or in vitro on GVBD or follicular contraction. Therefore, LPS did not appear to impair ovarian steroid production, oocyte final maturation or follicular contraction under the present experimental conditions. Interestingly, LPS administration in vivo induced apoptosis in follicular cells, an observation that correlated with changes in the expression of genes involved in apoptosis, as evidenced by microarray analysis.


          These results indicate that female trout are particularly resistant to an acute administration of LPS in terms of ovarian hormone responsiveness. However, LPS caused a marked increase in apoptosis in follicular cells, suggesting that the trout ovary could be sensitive to the pro-apoptotic effects of LPS-induced inflammatory cytokines.

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          Most cited references73

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          Macrophage contributions to ovarian function.

          Macrophages are multifunctional cells that play key roles in the immune response and are abundant throughout female reproductive tissues. Macrophages are identified in tissues by their expression of cell surface receptors and can execute diverse functional activities, including phagocytosis and degradation of foreign antigens, matrix dissolution and tissue remodelling, and production and secretion of cytokines, chemokines and growth factors. Their specific localization and variations in distribution in the ovary during different stages of the cycle, as well as their presence in peri-ovulatory human follicular fluid, suggest that macrophages play diverse roles in intra-ovarian events including folliculogenesis, tissue restructuring at ovulation and corpus luteum formation and regression. This review presents the existing evidence for the regulation of ovarian function by macrophages and macrophage-derived products, highlighting the implications of these cells in ovarian diseases, particularly polycystic ovary syndrome, endometriosis and premature ovarian failure.
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            Limiting inflammatory responses during activation of innate immunity.

            The idea of the importance of mounting an inflammatory response for effective immunity is supported by a multiplicity of experimental data. It is also well understood that resolution of inflammation is essential for maintaining the balance between health and disease. When the normal regulatory mechanisms are disturbed, the potential for developing chronic inflammatory diseases is increased. Inflammation is a key element in the response of the innate immune system to a variety of challenges, including those provided by bacterial and viral infection as well as by damaged or dying host cells. Here we review elements of innate immunity that lead to inflammation and some of the host mechanisms that allow for the resolution of the inflammatory responses.
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              The innate and early immune response to pathogen challenge in the female genital tract and the pivotal role of epithelial cells.

              A J Quayle (2015)
              The female reproductive tract is immunologically unique in its requirement for tolerance to allogeneic sperm and, in the upper tract, to the conceptus. However, it must also be appropriately protected from, and respond to, a diverse array of sexually transmitted pathogens. Some of these infections can be lethal (e.g. Human Immunodeficiency Virus (HIV), Human Papilloma Virus (HPV)), and others (e.g. Chlamydia trachomatis and Neisseria gonorrhoeae) can have potentially devastating reproductive sequelae. Interactions between a host and a pathogen are complex, diverse and regulated, and are a function of the individual pathogen, and host immunity. Although there is undoubtedly commonality in the mucosal immune response, there is also evidence of a degree of site-specificity in immune mechanisms, dependent upon the function and anatomical location of an organ. In this article, we review the evidence on the pivotal role of epithelial cells in the innate and early immune response to pathogen challenge in female genital tract tissues, and examine the evidence that the 'sterile' upper and the 'non-sterile' lower female genital tract may maintain a different immunological surveillance milieu, and may also respond differentially to pathogen challenge. We also review the unique characteristics, and subsequent ramifications of the acute cervical immune response to C. trachomatis, and discuss how natural antimicrobial mediators of immunity may be utilized to decrease the spread of sexually transmitted infections.

                Author and article information

                Reprod Biol Endocrinol
                Reproductive Biology and Endocrinology
                BioMed Central (London )
                31 August 2006
                : 4
                : 46
                [1 ]Departament de Fisiologia, Facultat de Biologia, Universitat de Barcelona, Barcelona, Spain
                [2 ]Unitat de Fisiologia Animal, Departament de Biologia Cellular, Fisiologia i d'Immunologia, Facultat de Ciencies, Universitat Autonoma de Barcelona, Bellaterra, Barcelona, Spain
                [3 ]Institute of Applied Biotechnology, University of Kuopio, Kuopio, Finland
                [4 ]Great Lakes Water Institute, University of Wisconsin-Milwaukee, Wisconsin, USA
                [5 ]Akvaforsk, PO Box 5010, N-1432 Ås, Norway
                Copyright © 2006 MacKenzie et al; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                : 1 June 2006
                : 31 August 2006

                Human biology
                Human biology


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