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863753V1.Full.Pdf bioRxiv preprint doi: https://doi.org/10.1101/863753; this version posted December 4, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 Belay et al Modulation of T helper 1 and T helper 2 immune balance in a stress mouse model during Chlamydia muridarum genital infection +Tesfaye Belay1, Elisha Martin1, Gezelle Brown1, Raenel Crenshaw1, Julia Street1#a, Ashleigh Freeman1#b, Shane Musick1#CTyler Kinder1#d 1Bluefield State College, Bluefield, WV 24701 #a Current address: Appalachian Regional Healthcare, Hinton, WV 25951 #b Current address: Princeton High School, Princeton, WV 24740 #c Current address: Medical School of Marshall University, Huntington, WV 25701 #d Current address: Dept of Molecular and Cellular Biochemistry, University of KY, Lexington, KY 40506 Running Title: Stress and Chlamydia muridarum genital infection Key words: T helper 1 & 2 cytokines, chlamydia, stress, mouse model Corresponding Author: +Tesfaye Belay, Bluefield State College, School of Arts and Sciences, 219 Rock Street, Bluefield, WV 24701. E-mail: [email protected] bioRxiv preprint doi: https://doi.org/10.1101/863753; this version posted December 4, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 2 Belay et al ABSTRACT A mouse model to study the effect of cold-induced stress on Chlamydia muridarum genital infection and immune response has been developed in our laboratory. Our previous results show that cold-induced stress increases the intensity of chlamydia genital infection, but little is known about the effect of cold-induced stress on differentiations and activities of T cell subpopulations and bone marrow derived dendritic cells (BMDCs). The factors that regulate the production of T helper 1 (Th1) or T helper 2 (Th2) cytokines is not clear. The objective of this study was to examine whether cold-induced stress modulates the expression of transcription factors and hallmark cytokines of Th1 and Th2 or differentiation of BMDCs during C. muridarum genital infection in mice. Our results show that mRNA level of beta2-adrenergic receptor (2-AR) compared to 1-AR and 3-AR was high in mixed population of CD4+ T cells and BMDCs. Further, decreased expression of T-bet and low level of interferon-gamma (IFN-) production and increased expression of GATA-3 and interleukin-4 (IL-4) production in CD4+ T of stressed mice was observed. Exposure of BMDCs to feroterol (2-AR agonist) or ICI,118551 (훽 2-AR antagonist), respectively, revealed significant stimulation or inhibition of 2-AR in stressed mice. Moreover, co-culturing of mature BMDC and naïve CD4+ T cells resulted in increased production of IL-4, IL-10, and IL-17 in culture supernatants, suggesting that stimulation of 2- AR leads to the increased production of Th2 cytokines. Overall, our results show for the first time that cold-induced stress is able to modulate the pattern of Th1 and Th2 cytokine environment, suggesting that it promotes the differentiation to Th2 rather than Th1 by the overexpression of GATA-3 correlated with elevated production of IL-4, IL-10, IL-23, and IL-17 in contrast to a low expression of T-bet correlated with less IFN- secretion in the mouse model. bioRxiv preprint doi: https://doi.org/10.1101/863753; this version posted December 4, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 3 Belay et al INTRODUCTION Chlamydia genital infection caused by Chlamydia trachomatis, the most common bacterial sexually transmitted disease (STD) worldwide [1] This infection, if left untreated, leads to the development of pelvic inflammatory disease (PID), fallopian tube scarring, ectopic pregnancy, infertility, and neonatal conjunctivitis [2,3]. Epidemiologic data from the Centers for Disease Control and Prevention and World Health Organization indicate that more than 90 and 4 million new cases occur annually worldwide and, in the US, respectively [4]. In the United States, chlamydia genital infection disproportionately affects populations of low socio-economic status, particularly African-Americans [5,6]. The reasons are not well known, but stress may have a major role in the persistent high rate of the disease associated with low socioeconomic conditions [7]. Several studies in animal models have demonstrated that anti-chlamydial T cell responses in the local genital mucosa play a role in the clearance of C. trachomatis from the genital tract [8- 12]. It is known that immunity to C. trachomatis is mediated by T-helper (Th), specifically T- helper 1 (Th1), cells through interferon-gamma (IFN-훾 ) -dependent and -independent pathways [13-16].Moreover, other studies in human subjects have identified and characterized factors that may be involved in the development of immunopathogenesis after chlamydia genital infection caused by the human strain C. trachomatis [17,18]. Those murine model studies have exhibited vital aspects of human genital chlamydial infection, including similar course of active infection, pathologic consequences or sequelae of an infection, tubal inflammation, hydrosalpinx formation and infertility [19-20]. It is well recognized that genital infection with C. trachomatis leads both to the recruitment of protective immune responses to the site of infection and infiltration of bioRxiv preprint doi: https://doi.org/10.1101/863753; this version posted December 4, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 4 Belay et al inflammatory products that may also contribute to pathological damage in the host [2, 21-23]. Repeated chlamydia genital infection in animal models [23-25] and human subjects [26, 27] is known to have a much greater risk of tubal obstruction than those with less exposure to C. trachomatis. Chlamydia muridarum, previously known as the mouse pneumonitis strain of C. trachomatis, is commonly used for the study of chlamydia immunity, pathogenesis and vaccine development [28, 29]. However, significant differences in the biology and pathogenesis of infections caused C. trachomatis and C. muridarum have been reported [30]. Mouse strain-dependent studies show that C. muridarum produces shorter courses of infection in C57BL/6 and BALB/c mice than in C3H/HeN mice, even though more resistance to oviduct pathology was observed in C57BL/6 mice [31]. A study has demonstrated the successful infectivity and elicitation of pathologies with both human and murine strains of Chlamydia in mice [32]. It is mostly agreed that no model is perfect, extensive literature reports suggest that immunological findings made using C. muridarum infection in mice is not vastly different from those that occur with C. trachomatis infections in humans [33]. Psychological or physical stress resulting from hardship of life in society has major impacts on public health [34-38]. Glucocorticoids and catecholamines are stress hormones that serve as the major mediators of stress responses by modulating signaling events, which result in either immunosuppression or immunostimulation in the host [39-41]. Norepinephrine (NE) is one of the catecholamines of the sympathetic nervous system released during stressful conditions including cold-water application [39, 42, 43]. Studies document the existence of at least eight different alpha or beta subtypes of NE receptors [44]. Norepinephrine binds and stimulates the bioRxiv preprint doi: https://doi.org/10.1101/863753; this version posted December 4, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 5 Belay et al beta2 adrenergic receptor (2-AR), which is predominantly expressed on CD4+ and B cells [45- 47]. Studies have further shown that production and direct binding of NE to 2-AR modulates immune responses, including altering cytokine production, lymphocyte proliferation, and antibody secretion [47-51]. More studies have shown that dendritic cells (DCs) have an essential role in the induction of T cell responses to clear C. muridarum during genital infection [29, 52]. Furthermore, DCs pulsed with a recombinant chlamydial major outer membrane protein antigen elicit a CD4(+) type T-helper 2 (Th2) rather than type Th1 immune response that is not protective [53]. Other studies have shown that transcription factors T-box expressed in T cells (T-bet) and GATA- binding protein-3 (GATA-3) and play important a regulation role in the differentiation of naive Th cells towards Th1 or Th2 cells in human subjects and animal models [18, 54]. Specifically, modulation of cytokines and transcription factors (T-bet and GATA-3 in CD4+ T cells of chlamydia patients was reported [18], but the expression patterns of T-bet and GATA-3 in CD4+ T cells in our stress model during chlamydia genital infection yet is unknown. Application of cold water as a stressor in animal models, including mice, has resulted in changes in immune responses that correlate with the activity of the neuroendocrine system of corticosteroids and catecholamines [55-60]. Although stress is implicated as a risk factor for various infections, its effect on chlamydia genital infection is unknown. We have previously shown that cold-water stress induces the production of catecholamines, which may play a critical role in the modulation of the immune system leading to increased intensity of C.
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