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      The Confluence of Sex Hormones and Aging on Immunity

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          Abstract

          The immune systems of post-pubescent males and females differ significantly with profound consequences to health and disease. In many cases, sex-specific differences in the immune responses of young adults are also apparent in aged men and women. Moreover, as in young adults, aged women develop several late-adult onset autoimmune conditions more frequently than do men, while aged men continue to develop many cancers to a greater extent than aged women. However, sex differences in the immune systems of aged individuals have not been extensively investigated and data addressing the effectiveness of vaccinations and immunotherapies in aged men and women are scarce. In this review, we evaluate age- and sex hormone-related changes to innate and adaptive immunity, with consideration about how this impacts age- and sex-associated changes in the incidence and pathogenesis of autoimmunity and cancer as well as the efficacy of vaccination and cancer immunotherapy. We conclude that future preclinical and clinical studies should consider age and sex to better understand the ways in which these characteristics intersect with immune function and the resulting consequences for autoimmunity, cancer, and therapeutic interventions.

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          Most cited references206

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          The X-files in immunity: sex-based differences predispose immune responses

          Sex-based differences in immune responses can influence the susceptibility to autoimmune and infectious diseases and the efficacy of therapeutic drugs. In this Perspective, Eleanor Fish discusses factors, such as X-linked genes, hormones and societal context, that underlie disparate immune responses in men and women.
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            Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication.

            Antibodies against nuclear self-antigens are characteristic of systemic autoimmunity, although mechanisms promoting their generation and selection are unclear. Here, we report that B cells containing the Y-linked autoimmune accelerator (Yaa) locus are intrinsically biased toward nucleolar antigens because of increased expression of TLR7, a single-stranded RNA-binding innate immune receptor. The TLR7 gene is duplicated in Yaa mice because of a 4-Megabase expansion of the pseudoautosomal region. These results reveal high divergence in mouse Y chromosomes and represent a good example of gene copy number qualitatively altering a polygenic disease manifestation.
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              A B-cell subset uniquely responsive to innate stimuli accumulates in aged mice.

              We have discovered a distinct mature B-cell subset that accumulates with age, which we have termed age-associated B cells. These cells comprise up to 30% of mature B cells by 22 months. Despite sharing some features with other mature B-cell subsets, they are refractory to BCR and CD40 stimulation. Instead, they respond to TLR9 or TLR7 stimulation and divide maximally on combined BCR and TLR ligation, leading to Ig production and preferential secretion of IL-10 and IL-4. Although similar to follicular B cells in both B-lymphocyte stimulator (BLyS) receptor expression and BLyS binding capacity, these cells do not rely on BLyS for survival. They are neither cycling nor the result of intrinsically altered B lymphopoiesis in aged BM, but instead appear to be generated from mature B cells that exhaustively expand during the individual's lifetime. Finally, they present Ag effectively and favor polarization to a TH17 profile. Together, these findings reveal that while the magnitude of the mature primary B-cell niche is maintained with age, it is increasingly occupied by cells refractory to BCR-driven activation yet responsive to innate receptor stimulation.

                Author and article information

                Contributors
                URI : https://frontiersin.org/people/u/495813
                URI : https://frontiersin.org/people/u/551647
                URI : https://frontiersin.org/people/u/265733
                Journal
                Front Immunol
                Front Immunol
                Front. Immunol.
                Frontiers in Immunology
                Frontiers Media S.A.
                1664-3224
                04 June 2018
                2018
                : 9
                : 1269
                Affiliations
                [1] 1Department of Biology, Randolph-Macon College , Ashland, VA, United States
                [2] 2W. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University , Baltimore, MD, United States
                Author notes

                Edited by: Virginia Rider, Pittsburg State University, United States

                Reviewed by: Piergiuseppe De Berardinis, Istituto di biochimica delle proteine (IBP), Italy; Paola Italiani, Consiglio Nazionale Delle Ricerche (CNR), Italy

                *Correspondence: Melanie R. Gubbels Bupp, melaniegubbelsbupp@ 123456rmc.edu

                Specialty section: This article was submitted to Cytokines and Soluble Mediators in Immunity, a section of the journal Frontiers in Immunology

                Article
                10.3389/fimmu.2018.01269
                5994698
                29915601
                ebcf8089-1d82-424a-af61-2056b9b7fe78
                Copyright © 2018 Gubbels Bupp, Potluri, Fink and Klein.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 19 March 2018
                : 22 May 2018
                Page count
                Figures: 1, Tables: 3, Equations: 0, References: 269, Pages: 15, Words: 5934
                Categories
                Immunology
                Review

                Immunology
                sex,sex hormones,immunity,autoimmunity,cancer,vaccines,immunotherapy,checkpoint blockade
                Immunology
                sex, sex hormones, immunity, autoimmunity, cancer, vaccines, immunotherapy, checkpoint blockade

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