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Try out PMC Labs and tell us what you think. Learn More. The role of sex hormones in regulating immune responses in the female genital tract has been recognized for decades. More recently, it has become increasingly clear that sex hormones regulate susceptibility to sexually transmitted infections through direct and indirect mechanisms involving inflammation and immune responses.

Exogenous hormones, such as those found in hormonal contraceptives, have come under intense scrutiny because of the increased susceptibility to sexually transmitted infections seen in women using medroxyprogesterone acetate, a synthetic progestin-based contraceptive. Recent studies describe a key role for the vaginal microbiota in determining susceptibility to sexually transmitted infections, including HIV While Lactobacillus spp.

Interestingly, sex hormones are inherently linked to microbiota regulation in the vaginal tract. Estrogen has been postulated to play a key role in establishing a Lactobacillus -dominated microenvironment, whereas medroxyprogesterone acetate is linked to hypo-estrogenic effects. The aim of this Review is to contribute to a better understanding of the sex-hormone—microbiome—immunity axis, which can provide key information on the determinants of HIV-1 susceptibility in the female genital tract and, consequently, inform HIV-1 prevention strategies.

Clinical and experimental evidence indicates that many sexually transmitted infections STIs are more prevalent in women than men Kaushic et al. There are both socio-economic and biological reasons why women may be more susceptible to STIs, including HIV-1, than men. The biological factors that could influence the outcome of pathogen exposure in the FGT include its large surface area, the alterations in physiology of reproductive tract tissues during different phases of the menstrual cycle, the influence of sex hormones on mucosal immune defense, the use of hormonal contraceptives and the effect of the indigenous microbiota see Box 1 for a glossary of terms.

In this Review, we highlight the mechanisms by which sex steroid hormones, including hormonal contraceptives, might impact the risk of HIV-1 susceptibility in women. The relevance of this area to public health is emphasized by the fact that more than 8 million women in sub-Saharan Africa, where HIV-1 is endemic, use DMPA as their main form of contraception Ross and Agwanda, In the context of this article, we are referring to the unique diversity of bacterial species found in the vaginal microbiota of each woman in our study.

Amsel criteria: a method to diagnose bacterial vaginosis BV. The Amsel criteria distinguish nonspecific vaginitis BV from other forms of vaginitis and from normal findings, as defined in Amsel et al.

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Antimicrobial peptides AMPs : part of the innate immune response for host defense, found in all classes of life. Cervical transformation zone: the area of the cervix where the columnar epithelial cells lining the endocervix change into the squamous epithelial cells lining the ectocervix; an area thought to be particularly prone to HIV-1 acquisition. Commensal: an organism living in relationship with another without harming or benefitting the host organism. Defensins: small proteins found in vertebrates and invertebrates that function as antimicrobial host defense peptides.

Estradiol E2 -based hormone replacement therapy HRT : treatment with natural or synthetic estrogens alone or in combination with progestins, typically aimed at alleviating the symptoms of menopause, or preventing osteoporosis. Ectocervix: the outer portion of the cervix that is located within the vaginal tract and lined by squamous epithelial cells. Elafin: a defensin antimicrobial peptide with antibacterial activity against bacterial and fungal pathogens.

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Also known as Trappin Lactoferrin: a defensin antimicrobial peptide that also binds iron. Lysozyme: a defensin antimicrobial protein that enzymatically cleaves and thus damages the components of the cell wall of Gram-positive bacteria. Microbiota: a consortium of bacteria residing in and on multicellular organisms, including plants and animals. Mucins: heavily glycosylated proteins glycoproteins produced by epithelial cells in most animals.

They are a constituent of vaginal mucus. A type of pattern recognition receptor PRR. Pattern recognition receptors PRRs : part of the innate immune system, these protein sensors detect pathogen-associated molecular patterns PAMPs and induce an innate response in the host. A chemotactic protein chemokine that recruits T cells, eosinophils and basophils, or other cells with cognate receptors. Seroconversion: the point at which a specific antibody has developed and become detectable in the peripheral blood i. Seronegative: a negative result in a blood test for antibodies against a certain virus or condition i.

HIV-1 or rheumatoid arthritis. Toll-like receptors TLRs : intra- or extracellular proteins that recognize microbes and nucleic acids, and participate in the innate immune response. The lower FGT, the vaginal tract and ectocervix Box 1is lined with epithelial cells covered by mucus and colonized by bacteria.

It is the first location encountered by HIV-1 during heterosexual intercourse with an infected male partner. The lower FGT provides a protective physical and immunological mucosal barrier. Acting as a structural support beneath the epithelium is a dense layer of stromal fibroblasts, in which a diverse population of leukocytes reside Wira et al.

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In order for HIV-1 transmission to occur, infectious virions must transverse the protective physical and immunological barriers of the FGT and infect target cells located in the stroma. While the exact mechanisms by which HIV-1 accesses target cells remain incompletely understood, this Review will focus on several factors known to influence HIV-1 susceptibility and acquisition in the FGT.

The lower FGT is lined with multi-layered squamous epithelial cells, and tight junctions linking these cells are mainly restricted to its basal layers. The epithelium in the lower FGT undergoes continuous differentiation, resulting in a mitotically active basal layer and a terminally differentiated superficial layer comprising cornified epithelial cells, which aid in preventing infection by certain pathogens, including HIV-1 Anderson et al. Aside from acting as a physical barrier, the vaginal epithelial cells also secrete mucins Box 1 into the vaginal lumen. These form a hydrophobic layer of mucus that traps pathogens and prevents access to the underlying epithelial cells Lai et al.

In addition to mucins, the vaginal mucus contains other host defense molecules, including antimicrobial peptides AMPs; Box 1 and complement system components, which can directly bind to and eliminate pathogens, impeding access to the vaginal epithelium Birse et al. These protective features can effectively dampen HIV-1 motility in human cervicovaginal mucus and enhance vaginal barrier function Shukair et al.

Colonizing the vaginal epithelium is an indigenous microbial community that can influence the physiology and immune function of the FGT Cruickshank and Sharman, ; Ma et al. The resident vaginal microbiota VMB exists in a mutualistic relationship with the female host and also participates in preventing vaginal infection by a variety of pathogens. The impact of the VMB on inflammation and susceptibility to HIV-1 is an emerging area of interest and will be discussed in more detail below.

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The upper FGT consists of the endocervix, uterus endometriumfallopian tubes and ovaries. It is lined by a single layer of epithelial cells linked by tight junctions that provide physical protection. It was originally believed that the upper FGT was sterile. However, like the vaginal tract, the upper FGT is colonized by bacteria Chen et al. Several studies have reported ificant correlation in microbial community members across the FGT, but their relative proportions vary Chen et al. Furthermore, the quantity of bacteria found on the endometrial surface are log orders of magnitude lower than those found in the vaginal tract Chen et al.

However, studies also identified many low-abundance genera Moreno et al. Similar to the VMB, the endometrial microbiota may be able to modulate inflammation. In vitro co-cultures of endometrial epithelial cells with pathogenic bacteria Neisseria gonorrhoeae induced proinflammatory mediators Christodoulides et al.

This suggests that the endometrial microbiota may be able to modulate endometrial inflammation in the host. In this Review, we discuss the recent information that is relevant to HIV-1 transmission in the lower FGT ectocervix and vaginawhich make up the major surface area exposed to HIVinfected semen during heterosexual intercourse. Although one of the main functions of the immune system in the FGT is to protect against an array of pathogens, it must concurrently allow for the main reproductive functions of the FGT, including supporting sperm migration, oocyte fertilization and embryo implantation.

To balance these unique requirements, the FGT is precisely regulated by the sex steroid hormones estradiol E2 and progesterone, which are cyclically produced by the ovaries throughout the menstrual cycle during the reproductive years in women Reed and Carr, ; Wira et al. Both fluctuating endogenous sex hormones and hormonal contraceptives can alter the components of the FGT defensive barriers, including mucus viscosity, epithelial barrier thickness, immune cell frequency and resident vaginal microbes Vitali et al.

For example, the amount and composition of the vaginal mucus varies with the menstrual cycle, hormonal contraceptive use, and hormone dampening at menopause Chappell et al. During ovulation, under the influence of estradiol, the vaginal mucus is thin with low viscosity, which facilitates sperm movement.

Conversely, during the progesterone-high luteal phase of the menstrual cycle, the vaginal mucus is thick and viscous, which impedes the movement of particulates from the lower to the upper FGT. Together, the carefully regulated fluctuations of these physicochemical features are necessary to promote both reproductive success and a robust defensive barrier in the FGT.

As these first lines of defense are heavily influenced by both hormones and microbiota composition, their dynamic interactions can substantially influence HIV-1 susceptibility in women, and will be discussed in detail below. In the lower FGT, epithelial cells, stromal fibroblasts and leukocytes interact with each other, with the sex hormones and with the VMB to induce the two arms of the immune response: innate and adaptive immunity Ferreira et al.

In addition to acting as a physical barrier against pathogens, the epithelial cells of the lower FGT modulate leukocyte function by producing cytokines and chemokines, which induce leukocyte differentiation and mediate inflammatory processes Fahey et al.

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Epithelial cells in both the upper and lower FGT Fig. Indeed, epithelial cells from both the upper and lower FGT have been reported to activate aling pathways following pathogen exposure Ferreira et al. In addition to inflammatory cytokines, cervicovaginal epithelial cells are known to produce AMPs, including defensins Box 1secretory leukocyte protease inhibitor SLPIlysozyme, lactoferrin and elafin Box 1 Nguyen et al.

Taken together, the epithelial cells of the lower FGT contribute to recognition of and defense against pathogens in part via their induction of inflammation and AMPs. Anatomy and immunological components of the female genital tract. The vaginal epithelium has many innate immune protection mechanisms, such as tight junctions, antimicrobial peptides AMPs and mucus, in order to neutralize, trap and prevent entry of potential pathogens. The vaginal lumen is colonized by commensal bacteria, mainly lactobacilli, which help to maintain a low pH. The abrupt transition from keratinized squamous epithelial cells of the ectocervix to single columnar epithelial cells of the endocervix represents the transformation zone; this site has an abundance of HIV-1 target cells and has been proposed to be one of the major sites for infections.

The presence of lymphoid aggregates in the endometrial tissue suggests that this is an inductive site for cell-mediated immunity. It was originally believed that the upper FGT was sterile; however, like the vaginal tract, the upper FGT is colonized by bacteria, including lactobacilli. Figure modified and reprinted with permission from Nguyen et al. TLR, Toll-like receptor. Residing in the lower FGT are numerous, dynamic leukocyte populations that contribute to humoral and cellular immunity.

For instance, flow cytometry measurements showed that primary vaginal macrophages were more susceptible to HIV-1 infection in vitro than gastrointestinal macrophages Shen et al. Leukocytes of the FGT are preferentially distributed in immunological microenvironments depending on their function within the FGT. Thus, while T cells are the main targets for HIV-1, macrophages and DCs can also be infected and therefore directly and indirectly affect HIV-1 susceptibility in women.

Most T cells in the lower FGT reside near the basal epithelial cell layer at the stromal cell interface; however, a large T-cell population also resides in the ectocervical and vaginal epithelium as intra-epithelial lymphocytes Pudney et al. In recent years, T-helper 17 Th17 cells have been identified as preferential targets for HIV-1 in the human cervix Cicala et al. Hence, the factors influencing the and activation of these cells can greatly impact HIV-1 susceptibility. Although B cells are a key cellular component of the adaptive immune system, they are not present in large s in the lower FGT.

Resident immunoglobulin A IgA -expressing plasma cells have been described in the cervix, especially in the endocervix Nguyen et al. In the case of IgG, the neonatal Fc receptor FcRN on genital epithelial cells facilitates transfer of IgG to the lumen to confer protection against vaginal infections Li et al. Even though relatively little is known about the role of B cells and antibodies in the FGT, in theory they have the potential to contribute to adaptive immunity and offer an additional layer of protection against HIV An overall summary of the general changes in immunity over the menstrual cycle are highlighted in Fig.

Changes in lower female genital tract immunity and HIV-1 susceptibility under endogenous and exogenous sex hormones. The endogenous levels of female sex hormones estradiol and progesterone vary throughout the day menstrual cycle in women. Estradiol dominates the follicular phase and reaches peak levels just prior to ovulation, which occurs around day Post-ovulation, estradiol levels decline as progesterone levels rise towards the mid-luteal phase.

A summary of the putative effects of hormones and hormonal contraceptives on female genital tract FGT immunity as presented in this Review are summarized as shown. Overall, while estradiol appears to promote factors related to decreased HIV-1 susceptibility, alterations in immunity during periods of high progesterone or DMPA use are associated with increased HIV-1 susceptibility.

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It is well documented that the endogenous female sex steroid hormones estradiol and progesterone, and their synthetic analogs, including those found in hormonal contraceptives, regulate immunity in the FGT. Other reviews provide a detailed of this immunoregulatory influence on immune cell phenotype and function Dunbar et al. In this article, we focus on the effect of endogenous and exogenous hormones in modulating key target cell populations, and thus HIV-1 susceptibility, in the lower FGT.

Although alterations in immune cell populations occur in endometrial tissues of the upper FGT Nguyen et al. However, other phenotypic and functional changes can occur within specific immune cell populations in response to sex hormones. Progesterone treatment of murine bone-marrow-derived DCs resulted in inhibited differentiation of DCs, leading to increased antigen uptake and decreased production of inflammatory cytokines, whereas opposing effects were observed after estradiol treatment Xiu et al. Collectively, these help illuminate the possible mechanisms by which progesterone might modulate immunity in the FGT and relate to HIV-1 susceptibility, which is greater in women in the progesterone-high luteal phase of the menstrual cycle Saba et al.

Although progesterone has been linked to increased HIV-1 susceptibility, estradiol can also impact immunity in the FGT. Depending on its concentration, estradiol can exert pro- or anti-inflammatory responses and differentially affect immune function Straub, In primary murine microglia and RAW Estradiol can also inhibit in vitro Th17 differentiation in mouse splenocytes Chen et al. Taken together, these suggest that estradiol typically maintains an anti-inflammatory immune environment that helps reduce susceptibility to infections while still maintaining the ability to mount an inflammatory, anti-viral response when necessary.

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In addition to the impact of endogenous sex steroid hormones on immunity in the FGT, exogenous hormones, such as those commonly found in hormonal contraceptives, can also affect immunity in the FGT.

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