Escape from X Chromosome Inactivation and the Female Predominance in Autoimmune Diseases

Laffont, 2019, Deconstructing the sex bias in allergy and autoimmunity: From sex hormones and beyond, Adv. Immunol., 142, 35, 10.1016/bs.ai.2019.04.001

NIH Autoimmune Diseases Coordinating Committee (ADCC) (2005, March 01). Progress in Autoimmune Diseases Research: Report to Congress. NIH publication number N° 05-5140 2005, Available online: https://www.niaid.nih.gov/sites/default/files/adccfinal.pdf.

Billi, 2019, Sex bias in autoimmunity, Curr. Opin. Rheumatol., 31, 53, 10.1097/BOR.0000000000000564

Fink, 2018, The evolution of greater humoral immunity in females than males: Implications for vaccine efficacy, Curr. Opin. Physiol., 6, 16, 10.1016/j.cophys.2018.03.010

Klein, 2016, Sex differences in immune responses, Nat. Rev. Immunol., 16, 626, 10.1038/nri.2016.90

Zuk, M. (2009). The sicker sex. PLoS Pathog., 5.

Bach, 2018, The hygiene hypothesis in autoimmunity: The role of pathogens and commensals, Nat. Rev. Immunol., 18, 105, 10.1038/nri.2017.111

Libert, 2010, The X chromosome in immune functions: When a chromosome makes the difference, Nat. Rev. Immunol., 10, 594, 10.1038/nri2815

Divekar, 2008, A role for sex chromosome complement in the female bias in autoimmune disease, J. Exp. Med., 205, 1099, 10.1084/jem.20070850

Sasidhar, 2012, The XX sex chromosome complement in mice is associated with increased spontaneous lupus compared with XY, Ann. Rheum. Dis., 71, 1418, 10.1136/annrheumdis-2011-201246

Scofield, 2008, Klinefelter’s syndrome (47,XXY) in male systemic lupus erythematosus patients: Support for the notion of a gene-dose effect from the X chromosome, Arthritis Rheumatol., 58, 2511, 10.1002/art.23701

Harris, 2016, Klinefelter’s syndrome (47,XXY) is in excess among men with Sjögren’s syndrome, Clin. Immunol., 168, 25, 10.1016/j.clim.2016.04.002

Fang, 2019, X Inactivation and Escape: Epigenetic and Structural Features, Front. Cell Dev. Biol., 7, 219, 10.3389/fcell.2019.00219

Graves, 1998, The origin and evolution of the pseudoautosomal regions of human sex chromosomes, Hum. Mol. Genet., 7, 1991, 10.1093/hmg/7.13.1991

Fish, 2008, The X-files in immunity: Sex-based differences predispose immune responses, Nat. Rev. Immunol., 8, 737, 10.1038/nri2394

Pinheiro, 2011, X-chromosome-located microRNAs in immunity: Might they explain male/female differences? The X chromosome-genomic context may affect X-located miRNAs and downstream signaling, thereby contributing to the enhanced immune response of females, Bioessays, 33, 791, 10.1002/bies.201100047

Barreiro, L.B., Ben-Ali, M., Quach, H., Laval, G., Patin, E., Pickrell, J.K., Bouchier, C., Tichit, M., Neyrolles, O., and Gicquel, B. (2009). Evolutionary dynamics of human Toll-like receptors and their different contributions to host defense. PLoS Genet., 5.

Simons, 2020, Presence of Genetic Variants among Young Men With Severe COVID-19, JAMA, 324, 663, 10.1001/jama.2020.13719

Carrel, 2005, X-inactivation profile reveals extensive variability in X-linked gene expression in females, Nature, 434, 400, 10.1038/nature03479

Tukiainen, 2017, Landscape of X chromosome inactivation across human tissues, Nature, 550, 244, 10.1038/nature24265

Wang, 2016, Unusual maintenance of X chromosome inactivation predisposes female lymphocytes for increased expression from the inactive X, Proc. Natl. Acad. Sci. USA, 113, E2029

Hagen, 2020, Heterogeneous Escape from X Chromosome Inactivation Results in Sex Differences in Type I IFN Responses at the Single Human pDC Level, Cell Rep., 33, 108485, 10.1016/j.celrep.2020.108485

Souyris, 2018, TLR7 escapes X chromosome inactivation in immune cells, Sci. Immunol., 3, eaap8855, 10.1126/sciimmunol.aap8855

Greenfield, 1998, The UTX gene escapes X inactivation in mice and humans, Hum. Mol. Genet., 7, 737, 10.1093/hmg/7.4.737

Heinz, 2020, TASL is the SLC15A4-associated adaptor for IRF5 activation by TLR7-9, Nature, 581, 316, 10.1038/s41586-020-2282-0

Souyris, 2019, Female predisposition to TLR7-driven autoimmunity: Gene dosage and the escape from X chromosome inactivation, Semin. Immunopathol., 41, 153, 10.1007/s00281-018-0712-y

Dhaliwal, 2019, TLR7 and TLR8 activate distinct pathways in monocytes during RNA virus infection, Sci. Signal., 12, eaaw1347, 10.1126/scisignal.aaw1347

Tripodo, 2018, Plasmacytoid dendritic cells promote systemic sclerosis with a key role for TLR8, Sci. Transl. Med., 10, eaam8458, 10.1126/scitranslmed.aam8458

Pisitkun, 2006, Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication, Science, 312, 1669, 10.1126/science.1124978

Deane, 2007, Control of toll-like receptor 7 expression is essential to restrict autoimmunity and dendritic cell proliferation, Immunity, 27, 801, 10.1016/j.immuni.2007.09.009

Guiducci, 2013, RNA recognition by human TLR8 can lead to autoimmune inflammation, J. Exp. Med., 210, 2903, 10.1084/jem.20131044

Christensen, 2006, Toll-like receptor 7 and TLR9 dictate autoantibody specificity and have opposing inflammatory and regulatory roles in a murine model of lupus, Immunity, 25, 417, 10.1016/j.immuni.2006.07.013

Theofilopoulos, 2017, The multiple pathways to autoimmunity, Nat. Immunol, 18, 716, 10.1038/ni.3731

Azar, 2020, TLR7 dosage polymorphism shapes interferogenesis and HIV-1 acute viremia in women, JCI Insight, 5, e136047, 10.1172/jci.insight.136047

Cotton, 2011, Chromosome-wide DNA methylation analysis predicts human tissue-specific X inactivation, Hum. Genet., 130, 187, 10.1007/s00439-011-1007-8

Odhams, 2019, Interferon inducible X-linked gene CXorf21 may contribute to sexual dimorphism in Systemic Lupus Erythematosus, Nat. Commun., 10, 2164, 10.1038/s41467-019-10106-2

Mackay, 2016, Molecular signatures in systemic lupus erythematosus: Distinction between disease flare and infection, Lupus Sci. Med., 3, e000159, 10.1136/lupus-2016-000159

Oghumu, 2019, Cutting Edge: CXCR3 Escapes X Chromosome Inactivation in T Cells during Infection: Potential Implications for Sex Differences in Immune Responses, J. Immunol., 203, 789, 10.4049/jimmunol.1800931

Trofa, 2018, CD40LG duplication-associated autoimmune disease is silenced by nonrandom X-chromosome inactivation, J. Allergy Clin. Immunol., 141, 2308, 10.1016/j.jaci.2018.02.010

Berletch, J.B., Ma, W., Yang, F., Shendure, J., Noble, W.S., Disteche, C.M., and Deng, X. (2015). Escape from X inactivation varies in mouse tissues. PLoS Genet., 11.

Itoh, 2019, The X-linked histone demethylase Kdm6a in CD4+ T lymphocytes modulates autoimmunity, J. Clin. Investig., 130, 3852, 10.1172/JCI126250

Dunford, 2017, Tumor-suppressor genes that escape from X-inactivation contribute to cancer sex bias, Nat. Genet., 49, 10, 10.1038/ng.3726

Brown, 1994, The human X-inactivation centre is not required for maintenance of X-chromosome inactivation, Nature, 368, 154, 10.1038/368154a0

Csankovszki, 2001, Synergism of Xist RNA, DNA methylation, and histone hypoacetylation in maintaining X chromosome inactivation, J. Cell Biol., 153, 773, 10.1083/jcb.153.4.773

Savarese, 2006, Hematopoietic precursor cells transiently reestablish permissiveness for X inactivation, Mol. Cell Biol., 26, 7167, 10.1128/MCB.00810-06

Syrett, C.M., Sindhava, V., Hodawadekar, S., Myles, A., Liang, G., Zhang, Y., Nandi, S., Cancro, M., Atchison, M., and Anguera, M.C. (2017). Loss of Xist RNA from the inactive X during B cell development is restored in a dynamic YY1-dependent two-step process in activated B cells. PLoS Genet., 13.

Syrett, 2019, Altered X-chromosome inactivation in T cells may promote sex-biased autoimmune diseases, JCI Insight, 4, e126751, 10.1172/jci.insight.126751

Syrett, 2019, Loss of epigenetic modifications on the inactive X chromosome and sex-biased gene expression profiles in B cells from NZB/W F1 mice with lupus-like disease, J. Autoimmun., 107, 102357, 10.1016/j.jaut.2019.102357

Adrianse, 2018, Perturbed maintenance of transcriptional repression on the inactive X-chromosome in the mouse brain after Xist deletion, Epigenetics Chromatin, 11, 50, 10.1186/s13072-018-0219-8

Ober, 2008, Sex-specific genetic architecture of human disease, Nat. Rev. Genet., 9, 911, 10.1038/nrg2415

Laffont, 2014, X-Chromosome complement and estrogen receptor signaling independently contribute to the enhanced TLR7-mediated IFN-alpha production of plasmacytoid dendritic cells from women, J. Immunol., 193, 5444, 10.4049/jimmunol.1303400

Valverde, 2012, TLR7/8/9 polymorphisms and their associations in systemic lupus erythematosus patients from southern Brazil, Lupus, 21, 302, 10.1177/0961203311425522

Pavlovic, 2010, Clinical and molecular evidence for association of SLE with parvovirus B19, Lupus, 19, 783, 10.1177/0961203310365715

Gonzalez-Quintial, R., Nguyen, A., Kono, D.H., Oldstone, M.B.A., Theofilopoulos, A.N., and Baccala, R. (2018). Lupus acceleration by a MAVS-activating RNA virus requires endosomal TLR signaling and host genetic predisposition. PLoS ONE, 13.

Griesbeck, 2015, Sex Differences in Plasmacytoid Dendritic Cell Levels of IRF5 Drive Higher IFN-alpha Production in Women, J. Immunol., 195, 5327, 10.4049/jimmunol.1501684