Sex-biased chromatin and regulatory cross-talk between sex chromosomes, autosomes, and mitochondria

Silkaitis, Katherine; Lemos, Bernardo

doi:10.1186/2042-6410-5-2

Cited by 39Genetic and Clinical Aspects of Sex Determination and Chromosomal AbnormalitiesGenomics and Chromatin DynamicsEpigenetics and DNA Methylation

Sex-biased chromatin and regulatory cross-talk between sex chromosomes, autosomes, and mitochondria

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Silkaitis, Katherine, Lemos, Bernardo·2014·Biology of Sex Differences

DOI 10.1186/2042-6410-5-2PMC PMC3907150

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Abstract

Several autoimmune and neurological diseases exhibit a sex bias, but discerning the causes and mechanisms of these biases has been challenging. Sex differences begin to manifest themselves in early embryonic development, and gonadal differentiation further bifurcates the male and female phenotypes. Even at this early stage, however, there is evidence that males and females respond to environmental stimuli differently, and the divergent phenotypic responses may have consequences later in life. The effect of prenatal nutrient restriction illustrates this point, as adult women exposed to prenatal restrictions exhibited increased risk factors of cardiovascular disease, while men exposed to the same condition did not. Recent research has examined the roles of sex-specific genes, hormones, chromosomes, and the interactions among them in mediating sex-biased phenotypes. Such research has identified testosterone, for example, as a possible protective agent against autoimmune disorders and an XX chromosome complement as a susceptibility factor in murine models of lupus and multiple sclerosis. Sex-biased chromatin is an additional and likely important component. Research suggesting a role for X and Y chromosome heterochromatin in regulating epigenetic states of autosomes has highlighted unorthodox mechanisms of gene regulation. The crosstalk between the Y chromosomes and autosomes may be further mediated by the mitochondria. The organelles have solely maternal transmission and exert differential effects on males and females. Altogether, research supports the notion that the interaction between sex-biased elements might exert novel regulatory functions in the genome and contribute to sex-specific susceptibilities to autoimmune and neurological diseases.

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Sexual dimorphism in mitochondrial function has been related to genetic interactions between sex chromosomes and autosomes.
“Although sexual dimorphism in mitochondrial function have been related to the genetic interactions between sex chromosomes and autosomes (114, 115).”
From From mitochondria to sarcopenia: role of 17β-estradiol and testosterone (2023) · cites this paper as [114]

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Lemos, B., Branco, A. T., & Hartl, D. L. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010383107 · Cited by 173 · cited 2× · see citing works
“Aside from the disproportionate modulation of genes that code for protein products that localize to the nucleus and which might modify chromatin dynamics, there is a substantial contribution of Y chromosome origin to the differential expression of immune response genes [79,98,111].”
Background
Androgens are protective in experimental autoimmune encephalomyelitis: implications for multiple sclerosis
Palaszynski, K. M., Loo, K. K., Ashouri, J. F., Liu, H.-B., & Voskuhl, R. R. (2003) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2003.11.004 · Cited by 171 · cited 1× · see citing works
“This result echoes earlier murine research in which the effect of androgen removal on EAE was dependent on genetic background [118], and observations that autosomal gene associations with MS susceptibility are often sex-specific in humans [119,120].”
Result
Ribosomal DNA Deletions Modulate Genome-Wide Gene Expression: “rDNA–Sensitive” Genes and Natural Variation
Paredes, S., Branco, A. T., Hartl, D. L., Maggert, K. A., & Lemos, B. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1001376 · Cited by 166 · cited 1× · see citing works
“melanogaster, the Y chromosome also contains variation in repeat number of the multi-copy rDNA locus, which leads to both differential PEV and global gene expression [99].”
Background
Low conservation of gene content in the Drosophila Y chromosome
Koerich, L. B., Wang, X., Clark, A. G., & Carvalho, A. B. (2008) · Nature · doi:10.1038/nature07463 · Cited by 164 · cited 2× · see citing works
“protein-coding genes and accounts for nearly 25% of male haploid DNA content [89,90]; in contrast, the X”
Background
Epigenetic regulation of autosomal gene expression by sex chromosomes
Wijchers, P. J., & Festenstein, R. (2011) · Trends in Genetics · doi:10.1016/j.tig.2011.01.004 · Cited by 164 · cited 3× · see citing works
“The regulation may be due to a direct transcriptional role of Sry or it may be mediated by sex hormones; the latter is supported by research indicating that XY complement-induced differences in immune response might be suppressed in the presence of testosterone [77].”
BackgroundInfluential
Heat induced male sterility inDrosophila melanogaster: adaptive genetic variations among geographic populations and role of the Y chromosome
Rohmer, C., David, J. R., Moréteau, B., & Joly, D. (2004) · Journal of Experimental Biology · doi:10.1242/jeb.01087 · Cited by 159 · see citing works
Carrier Detection in X-Linked Agammaglobulinemia by Analysis of X-Chromosome Inactivation
Fearon, E. R., Winkelstein, J. A., Civin, C. I., Pardoll, D. M., & Vogelstein, B. (1987) · New England Journal of Medicine · doi:10.1056/nejm198702193160802 · Cited by 158 · cited 1× · see citing works
“globulinemia, an X-linked immune deficiency, exhibit non-random XCI in B cell lymphocytes [48], and female carriers of Wiskott-Aldrich syndrome exhibit nonrandom inactivation in all blood cell lineages [49].”
Background
Autoimmunity and Klinefelter's syndrome: When men have two X chromosomes
Sawalha, A. H., Harley, J. B., & Scofield, R. H. (2009) · Journal of Autoimmunity · doi:10.1016/j.jaut.2009.03.006 · Cited by 156 · cited 1× · see citing works
“The Y-linked autoimmune acceleration (Yaa) locus in male mice contains a translocation that includes toll-like receptor 7 from the X chromosome and contributes to a severe lupus-like phenotype in some mice strains [23].”
Background
Y chromosome polymorphism is a strong determinant of male fitness in Drosophila melanogaster
Chippindale, A. K., & Rice, W. R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.101456898 · Cited by 155 · cited 1× · see citing works
“to temperature, fertility, spermatogenesis, and fitness, as well as the expression of hundreds of X-linked and autosomal genes [92-95].”
Background
The Y chromosome as a regulatory element shaping immune cell transcriptomes and susceptibility to autoimmune diseasePreprint
Case, L. K., Wall, E. H., Dragon, J. A., Saligrama, N., Krementsov, D. N., Moussawi, M., Zachary, J. F., Huber, S. A., Blankenhorn, E. P., & Teuscher, C. (2013) · Genome Research · doi:10.1101/gr.156703.113 · Cited by 146 · see citing works
Blastocysts prepare for the race to be male
Mittwoch, U. (1993) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a137889 · Cited by 141 · cited 1× · see citing works
“Finally, evidence suggests that prior to differentiation of the gonads and production of sex hormones, male pre-implantation embryos are larger than those of females [61,62], and some genes, located on both autosomes and sex chromosomes, are already differentially expressed between the two sexes at that stage [63,64].”
Background
A paternally imprinted X chromosome retards the development of the early mouse embryo
Thornhill, A. R., & Burgoyne, P. S. (1993) · Development · doi:10.1242/dev.118.1.171 · Cited by 134 · see citing works
Sexual Dimorphism in Mammalian Autosomal Gene Regulation Is Determined Not Only by Sry but by Sex Chromosome Complement As Well
Wijchers, P. J., Yandım, C., Panousopoulou, E., Ahmad, M., Harker, N., Saveliev, A., Burgoyne, P. S., & Festenstein, R. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.08.005 · Cited by 134 · cited 10× · see citing works
“The extent of silencing appeared determined by sex chromosome complement independent of gonadal sex [60].”
BackgroundInfluential
Gonadal hormones influence the immune response to PLP 139–151 and the clinical course of relapsing experimental autoimmmune encephalomyelitis
Bebo, B. F., Zelinka-Vincent, E., Adamus, G., Amundson, D., Vandenbark, A. A., & Offner, H. (1998) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(97)00214-2 · Cited by 130 · see citing works
X and Y Chromosome Complement Influence Adiposity and Metabolism in Mice
Chen, X., McClusky, R., Itoh, Y., Reue, K., & Arnold, A. P. (2013) · Endocrinology · doi:10.1210/en.2012-2098 · Cited by 130 · see citing works
Association between nonrandom X-chromosome inactivation and BRCA1 mutation in germline DNA of patients with ovarian cancer.
Buller, R., Sood, A., Lallas, T., Buekers, T., & Skilling, J. (1999) · Journal of the National Cancer Institute · doi:10.1093/jnci/91.4.339 · Cited by 129 · cited 1× · see citing works
“Skewed XCI has also been suggested to play a role in disease pathogenesis, such as that of systemic sclerosis (SSc) [50], and it has been documented in breast and ovarian cancers [51,52].”
Background
Nonrandom inactivation of the X chromosome in early lineage hematopoietic cells in carriers of Wiskott-Aldrich syndrome
Wengler, G., Gorlin, J. B., Williamson, J., Rosen, F. S., & Bing, D. (1995) · Blood · doi:10.1182/blood.v85.9.2471.bloodjournal8592471 · Cited by 127 · cited 1× · see citing works
“globulinemia, an X-linked immune deficiency, exhibit non-random XCI in B cell lymphocytes [48], and female carriers of Wiskott-Aldrich syndrome exhibit nonrandom inactivation in all blood cell lineages [49].”
Background
Transcription of the Y chromosomal gene,Sry, in adult mouse brain
Lahr, G., Maxson, S. C., Mayer, A., Just, W., Pilgrim, C., & Reisert, I. (1995) · Molecular Brain Research · doi:10.1016/0169-328x(95)00136-g · Cited by 123 · cited 1× · see citing works
“Sry is also notably important in the brain [31,32].”
Background
Y chromosome loss in male patients with primary biliary cirrhosis
Lleò, A., Oertelt‐Prigione, S., Bianchi, I., Caliari, L., Finelli, P., Miozzo, M. R., Lazzari, R., Floreani, A., Donato, F., Colombo, M., et al. (2013) · Journal of Autoimmunity · doi:10.1016/j.jaut.2012.12.008 · Cited by 113 · see citing works
Sex of the cell dictates its response: differential gene expression and sensitivity to cell death inducing stress in male and female cells
Penaloza, C. G., Estevez, B., Orlanski, S., Sikorska, M., Walker, R., Smith, C. C., Smith, B., Lockshin, R. A., & Zakeri, Z. F. (2009) · The FASEB Journal · doi:10.1096/fj.08-119388 · Cited by 111 · cited 2× · see citing works
“The data suggested that sex chromosome complement underlies the differential sensitivity of male and female embryonic cells to some stressors, with the introduction of hormonal secretions functioning as a modifier of those differences [78].”
Background
Regulation of monoamine oxidase A by the SRY gene on the Y chromosome
Wu, J. B., Chen, K., Li, Y., Lau, Y. C., & Shih, J. C. (2009) · The FASEB Journal · doi:10.1096/fj.09-139097 · Cited by 110 · cited 1× · see citing works
“MAO A plays a critical role in brain development and function, and its abnormal activity has been suggested in sex-biased neurological disorders, such as autism, depression, and attention deficit hyperactivity disorder [34].”
Background
What a Difference an X or Y Makes: Sex Chromosomes, Gene Dose, and Epigenetics in Sexual Differentiation
Arnold, A. P., Chen, X., & Itoh, Y. (2012) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-30726-3_4 · Cited by 105 · see citing works
The human testis‐determining factor SRY localizes in midbrain dopamine neurons and regulates multiple components of catecholamine synthesis and metabolism
Czech, D., Lee, J., Sim, H., Parish, C. L., Vilain, E. J. N., & Harley, V. R. (2012) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2012.07782.x · Cited by 101 · see citing works
Developmental Consequences of Sexual Dimorphism During Pre‐implantation Embryonic Development
Gutiérrez‐Adán, A., Perez‐Crespo, M., Fernández‐González, R., Ramirez, M., Moreira, P., Pintado, B., Lonergan, P., & Rizos, D. V. (2006) · Reproduction in Domestic Animals · doi:10.1111/j.1439-0531.2006.00769.x · Cited by 97 · cited 1× · see citing works
“Finally, evidence suggests that prior to differentiation of the gonads and production of sex hormones, male pre-implantation embryos are larger than those of females [61,62], and some genes, located on both autosomes and sex chromosomes, are already differentially expressed between the two sexes at that stage [63,64].”
Background
Position effect variegation in Drosophila melanogaster: relationship between suppression effect and the amount of Y chromosome.
Dimitri, P., & Pisano, C. (1989) · Genetics · doi:10.1093/genetics/122.4.793 · Cited by 94 · see citing works
Increased loss of the Y chromosome in peripheral blood cells in male patients with autoimmune thyroiditis
Persani, L., Bonomi, M., Lleò, A., Pasini, S. M., Civardi, F., Bianchi, I., Campi, I., Finelli, P., Miozzo, M. R., Castronovo, C., et al. (2011) · Journal of Autoimmunity · doi:10.1016/j.jaut.2011.11.011 · Cited by 92 · cited 1× · see citing works
“chromosome loss in peripheral blood cells, and women with primary biliary cirrhosis display increased rates of X monosomy [45,55].”
Background
The XX sex chromosome complement in mice is associated with increased spontaneous lupus compared with XY
Manda, S. V., Itoh, N., Gold, S. M., Lawson, G. W., & Voskuhl, R. R. (2012) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2011-201246 · Cited by 92 · cited 1× · see citing works
“Additionally, an XX complement in mice, independent of gonadal sex, can increase the risk of lupus and experimental autoimmune encephalomyelitis (EAE; a mouse model of MS) when compared to an XY complement independent of gonadal sex [20,54].”
Background
The Immunogenetic Architecture of Autoimmune DiseasePreprint
Goris, A., & Liston, A. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a007260 · Cited by 90 · cited 1× · see citing works
“While research identifying loci contributing to sexbiased phenotypes has helped discern disease mechanisms and improve susceptibility assessment in populations and individuals, there are few sex-biased diseases that follow a simple Mendelian inheritance pattern [25].”
Background
Dysregulation of the hypothalamic–pituitary–gonadal axis in experimental autoimmune encephalomyelitis and multiple sclerosis
Foster, S. C., Daniels, C., BOURDETTE, D. N., & Bebo, B. F. (2003) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(03)00177-2 · Cited by 87 · cited 1× · see citing works
“levels during the height of the disease [117].”
Background
High frequency of skewed X inactivation in young breast cancer patients
Kristiansen, M. B., Langerød, A., Knudsen, G. P., Weber, B. L., Børresen-Dale, A.-L., & Ørstavik, K. H. (2002) · Journal of Medical Genetics · doi:10.1136/jmg.39.1.30 · Cited by 86 · see citing works
What about gr/gr deletions and male infertility? Systematic review and meta-analysis
Stouffs, K., Lissens, W., Tournaye, H. J., & Haentjens, P. (2010) · Human Reproduction Update · doi:10.1093/humupd/dmq046 · Cited by 86 · cited 1× · see citing works
“For instance, a specific deletion in the Y chromosome contributes to male infertility in some human populations, but not others [88], suggesting interactions with the genetic background.”
Background
Sex-specific role of Drosophila melanogaster HP1 in regulating chromatin structure and gene transcription
Liu, L., Ni, J., Shi, Y., Oakeley, E. J., & Sun, F.-L. (2005) · Nature Genetics · doi:10.1038/ng1662 · Cited by 80 · cited 1× · see citing works
“The protein appears to exert sex-specific gene regulation in Drosophila, and deletion causes sexbiased lethality [104].”
Background
How Do Y-Chromosomes Modulate Genome-Wide Epigenetic States: Genome Folding, Chromatin Sinks, and Gene Expression
Francisco, F. D. O., & Lemos, B. (2014) · Journal of Genomics · doi:10.7150/jgen.8043 · Cited by 73 · cited 2× · see citing works
“Genes responsive to the Y chromosome may show restricted nuclear distribution, although the arrangement is bound to be variable across cell types [100].”
Background
Transcriptional sexual dimorphism in elongating bovine embryos: implications for XCI and sex determination genes
Bermejo‐Álvarez, P., Rizos, D. V., Lonergan, P., & Gutiérrez‐Adán, A. (2011) · Reproduction · doi:10.1530/rep-11-0006 · Cited by 72 · cited 1× · see citing works
“Finally, evidence suggests that prior to differentiation of the gonads and production of sex hormones, male pre-implantation embryos are larger than those of females [61,62], and some genes, located on both autosomes and sex chromosomes, are already differentially expressed between the two sexes at that stage [63,64].”
Background
Cutting Edge: The Y Chromosome Controls the Age-Dependent Experimental Allergic Encephalomyelitis Sexual Dimorphism in SJL/J Mice
Spach, K. M., Blake, M., Bunn, J. Y., McElvany, B. D., Noubade, R., Blankenhorn, E. P., & Teuscher, C. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0803200 · Cited by 71 · see citing works
NUCLEAR-MITOCHONDRIAL EPISTASIS FOR FITNESS IN SACCHAROMYCES CEREVISIAE
Zeyl, C., Andreson, B., & Weninck, E. (2005) · Evolution · doi:10.1111/j.0014-3820.2005.tb01764.x · Cited by 68 · cited 1× · see citing works
“Evidence of coevolution of the male mitochondrial genome with the nuclear genome is abundant [10,85,86].”
Background
YNot a Dead End: Epistatic Interactions BetweenY-Linked Regulatory Polymorphisms and Genetic Background Affect Global Gene Expression inDrosophila melanogaster
Jiang, P., Hartl, D. L., & Lemos, B. (2010) · Genetics · doi:10.1534/genetics.110.118109 · Cited by 66 · cited 1× · see citing works
“Aside from the disproportionate modulation of genes that code for protein products that localize to the nucleus and which might modify chromatin dynamics, there is a substantial contribution of Y chromosome origin to the differential expression of immune response genes [79,98,111].”
Background
Chromosome Y Regulates Survival Following Murine Coxsackievirus B3 Infection
Case, L. K., Toussaint, L. E., Moussawi, M., Roberts, B., Saligrama, N., Brossay, L., Huber, S. A., & Teuscher, C. (2012) · G3 Genes Genomes Genetics · doi:10.1534/g3.111.001610 · Cited by 65 · see citing works
Sex ratio of multiple sclerosis in the National Swedish MS Register (SMSreg)
Boström, I., Stawiarz, L., & Landtblom, A. (2012) · Multiple Sclerosis Journal · doi:10.1177/1352458512446169 · Cited by 64 · see citing works
The X in sex: how autoimmune diseases revolve around sex chromosomes
Selmi, C. F. (2008) · Best Practice & Research Clinical Rheumatology · doi:10.1016/j.berh.2008.09.002 · Cited by 64 · cited 1× · see citing works
“Mutations, deletions, and translocations involving the X chromosome have also been linked to disease phenotypes with a sex bias, including mutations in the WAS gene that cause Wiskott-Aldrich syndrome and mutations in IL2RG that cause X-linked recessive severe combined immunodeficiency syndrome [22].”
Background
Influence of sex chromosome constitution on the genomic imprinting of germ cells
Durcova‐Hills, G., Hájková, P., Sullivan, S. K., Barton, S. C., Surani, M. A., & McLaren, A. L. D. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602621103 · Cited by 63 · cited 1× · see citing works
“DNA methylation of imprinted alleles in germ cells is influenced by sex chromosome complement as well as the gonadal sex of the embryo [57].”
Background
IFNG polymorphisms are associated with gender differences in susceptibility to multiple sclerosis
Kantarci, O. H., Goris, A., Hebrink, D. D., Heggarty, S., Cunningham, S., Alloza, I., Atkinson, E. J., de Andrade, M., McMurray, C. T., Graham, C. A., et al. (2005) · Genes and Immunity · doi:10.1038/sj.gene.6364164 · Cited by 63 · cited 1× · see citing works
“This result echoes earlier murine research in which the effect of androgen removal on EAE was dependent on genetic background [118], and observations that autosomal gene associations with MS susceptibility are often sex-specific in humans [119,120].”
Result
Sex-specific responses to stroke
Turtzo, L. C., & McCullough, L. D. (2009) · Future Neurology · doi:10.2217/fnl.09.66 · Cited by 60 · cited 1× · see citing works
“Studies have documented variable incidence of infection in male and female children [1], disproportionate female susceptibility to immune diseases [2,3], greater risk of mental illness and overall mortality in males [4], variable cancer rates between the sexes [5,6], sex-specific risk for stroke and diseases of aging…”
Background
Pregnancy and Multiple Sclerosis
Houtchens, M. K. (2007) · Seminars in Neurology · doi:10.1055/s-2007-991127 · Cited by 57 · see citing works
Rapid evolution of mouse Y centromere repeat DNA belies recent sequence stabilityPreprint
Pertile, M. D., Graham, A. N., Choo, K. H. A., & Kalitsis, P. (2009) · Genome Research · doi:10.1101/gr.092080.109 · Cited by 53 · cited 4× · see citing works
“Kantarci O, Goris A, Hebrink D, Heggarty S, Cunningham S, Alloza I, Atkinson E, de Andrade M, McMurray C, Graham C, Hawkins S, Billiau A, Dubois B, Weinshenker B, Vandenbroeck K: IFNG polymorphisms are associated with gender differences in susceptibility to multiple sclerosis.”
MethodInfluential
Gene dosage compensation in metafemales (3X; 2A) of Drosophila
Lucchesi, J. C., Rawls, J. M., & Maroni, G. (1974) · Nature · doi:10.1038/248564a0 · Cited by 44 · cited 1× · see citing works
“The n sterile and can display narrowed abdomens, wing abnormalities, irregular , and viability post-eclosion is limited [72-75].”
Background
Gene expression in adult metafemales of Drosophila melanogaster.
Birchler, J. A., Hiebert, J. C., & Krietzman, M. (1989) · Genetics · doi:10.1093/genetics/122.4.869 · Cited by 44 · see citing works
The delicate balance between male and female sex determining pathways: potential for disruption of early steps in sexual development
Koopman, P. A. (2009) · International Journal of Andrology · doi:10.1111/j.1365-2605.2009.01001.x · Cited by 39 · cited 2× · see citing works
“The cascade eliminates the Müllerian ducts, which would otherwise develop into the oviduct and uterus [28,30].”
Background
Transcription modulation chromosome-wide: universal features and principles of dosage compensation in worms and flies
Straub, T., & Becker, P. B. (2011) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2011.01.012 · Cited by 36 · cited 2× · see citing works
“Drosophila males, meanwhile, express X chromosome genes at twice the rate as females, and mammalian females use X inactivation as a dosage compensation mechanism [39,53] (Figure 1).”
Background
Roles for Mating and Environment in C. elegans Sex Determination
Prahlad, V., Pilgrim, D. B., & Goodwin, E. B. (2003) · Science · doi:10.1126/science.1087946 · Cited by 32 · see citing works
Recent advances in X-chromosome inactivation
Kalantry, S. (2011) · Journal of Cellular Physiology · doi:10.1002/jcp.22673 · Cited by 30 · see citing works
Erratum: Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production (Science (2007) (121))
Naugler, W. E. (2009) · Science · Cited by 30 · see citing works
Gender-Associated Differences of Perforin Polymorphisms in the Susceptibility to Multiple Sclerosis
Camiña-Tato, M., Morcillo-Suárez, C., Bustamante, M. F., Ortega, I. C., Navarro, A., Muntasell, A., López‐Botet, M., Sánchez‐Pla, Á., Carmona, P., Julià, E., et al. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1000102 · Cited by 29 · cited 1× · see citing works
“This result echoes earlier murine research in which the effect of androgen removal on EAE was dependent on genetic background [118], and observations that autosomal gene associations with MS susceptibility are often sex-specific in humans [119,120].”
Result
Y Chromosome–Linked B and NK Cell Deficiency in Mice
Sun, S., Horino, S., Itoh‐Nakadai, A., Kawabe, T., Asao, A., Takahashi, T., So, T., Funayama, R., Kondo, M., Saitsu, H., et al. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1300303 · Cited by 20 · see citing works
Association study of TRAF1/C5 polymorphism (rs10818488) with susceptibility to rheumatoid arthritis and systemic lupus erythematosus: A meta-analysis
Xu, K., Peng, H., Zhou, M., Wang, W., Li, R., Zhu, K.-K., Zhang, M., Wen, P., Pan, H., & Ye, D. (2013) · Gene · doi:10.1016/j.gene.2012.12.092 · Cited by 18 · cited 1× · see citing works
“Similarly, the TRAF1/C5 polymorphism has been implicated in susceptibility to RA in a North African population and with susceptibility to SLE in a European population [82].”
Background
Chromosome Y variants from different inbred mouse strains are linked to differences in the morphologic and molecular responses of cardiac cells to postpubertal testosterone
Llamas, B., Verdugo, R. A., Churchill, G. A., & Deschepper, C. F. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-150 · Cited by 18 · cited 3× · see citing works
“Finally, recent research points toward a role for the Y chromosome in regulating cardiac phenotypes, neonatal programming, and chromatin structure in mice [122,123].”
Background
Novel Effects of Chromosome Y on Cardiac Regulation, Chromatin Remodeling, and Neonatal Programming in Male Mice
Praktiknjo, S. D., Llamas, B., Scott‐Boyer, M., Picard, S., Robert, F., Langlais, D., Haibe‐Kains, B., Faubert, D., Silversides, D. W., & Deschepper, C. F. (2013) · Endocrinology · doi:10.1210/en.2013-1699 · Cited by 13 · cited 2× · see citing works
“Finally, recent research points toward a role for the Y chromosome in regulating cardiac phenotypes, neonatal programming, and chromatin structure in mice [122,123].”
Background
Rheumatoid arthritis in Senegal: a comparison between patients coming from rural and urban areas, in an urban tertiary health care center in Senegal
Lekpa, F. K., Ndongo, S., Tiendrébéogo, J., Ndao, A. C., Daher, A., Pouye, A., Ka, M. M., & Diop, T. M. (2012) · Clinical Rheumatology · doi:10.1007/s10067-012-2054-9 · Cited by 13 · cited 1× · see citing works
“The increased prevalence of RA in urban Senegalese populations compared to their rural counterparts suggests environmental triggers in otherwise healthy but genetically susceptible population [81].”
Background
Chromatin-Associated Proteins HP1 and Mod(mdg4) Modify Y-Linked Regulatory Variation in the Drosophila Testis
Branco, A. T., Hartl, D. L., & Lemos, B. (2013) · Genetics · doi:10.1534/genetics.113.150805 · Cited by 11 · cited 1× · see citing works
“[101] recently showed that the manifestation of variable Y chromosomes on gene expression requires wild-type function of the heterochromatin protein 1 (HP1).”
Background
The epidemiology of Turner syndrome
Gravholt, C. H., & Stochholm, K. (2006) · International Congress Series · doi:10.1016/j.ics.2006.06.009 · Cited by 10 · cited 1× · see citing works
“ve female external genitals but often have non-functioning ovaries, lack a females [68].”
Background
Age-specific sex ratio of multiple sclerosis in the National Swedish MS Register (SMSreg)
Boström, I., Stawiarz, L., & Landtblom, A. (2013) · Multiple Sclerosis Journal · doi:10.1177/1352458513498636 · Cited by 7 · cited 1× · see citing works
“In humans, MS is more prevalent in women, and the ratio of women to men appears to be increasing [113-115].”
Background
THE OCCURRENCE OF PARTIALLY FERTILE TRIPLOID METAFEMALES IN DROSOPHILA MELANOGASTER
Frost, J. N. (1960) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.46.1.47 · Cited by 6 · cited 1× · see citing works
“The n sterile and can display narrowed abdomens, wing abnormalities, irregular , and viability post-eclosion is limited [72-75].”
Background
Chromosomal Sex Determination in Mammals
Gilbert, S. F. (2000) · Cited by 5 · see citing works
Chromosomal Sex Determination in Drosophila
Gilbert, S. F. (2000) · Cited by 5 · see citing works
RESPONSE: Re: Association Between Nonrandom X-Chromosome Inactivation and BRCA1 Mutation in Germline DNA of Patients With Ovarian Cancer
Buller, R. E., Sood, A. K., Lallas, T. A., Buekers, T., & Skilling, J. S. (1999) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/91.17.1508 · Cited by 5 · see citing works
Primordial Germ Cells and Sex Determination in Mammals
Alberts, B., Johnson, A. A. T., Lewis, J., RAFF, M. C., Roberts, K., & Walter, P. (2002) · Cited by 4 · see citing works
Some Environmental Influences on Metafemale Viability in Drosophila melanogaster
Neeley, J. C. (1971) · Journal of Heredity · doi:10.1093/oxfordjournals.jhered.a108187 · Cited by 3 · cited 1× · see citing works
“The n sterile and can display narrowed abdomens, wing abnormalities, irregular , and viability post-eclosion is limited [72-75].”
Background

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Sorted by citations

Mechanistic Pathways of Sex Differences in Cardiovascular Disease
Regitz‐Zagrosek, V., & Kararigas, G. (2016) · Physiological Reviews · doi:10.1152/physrev.00021.2015 · Cited by 738 · see citing works
“They have been postulated to contribute to sex-specific susceptibilities to autoimmune and neurological diseases (361).”
Background
Mitochondria: A central target for sex differences in pathologies
Ventura-Clapier, R., Moulin, M., Piquereau, J., Lemaire, C., Mericskay, M., Veksler, V., & Garnier, A. (2017) · Clinical Science · doi:10.1042/cs20160485 · Cited by 371 · see citing works
A general theory of sexual differentiation
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REVIEW
(2016)
A role for sex chromosome complement in the female bias in autoimmune disease
Smith-Bouvier, D. L., Divekar, A., Manda, S. V., Du, S., Tiwari-Woodruff, S. K., King, J. K., Arnold, A. P., Singh, R. R., & Voskuhl, R. R. (2008) · The Journal of Experimental Medicine · doi:10.1084/jem.20070850 · Cited by 398 · see citing works
Sex differences in autoimmune disorders: Inspecting the roles of the X chromosome
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POS0360 X-CHROMOSOME DOSAGE, RATHER THAN THE GONADAL SEX ITSELF, MAJORLY CONTRIBUTES TO SEX BIAS IN AUTOIMMUNITY IN HUMANS
Singh, R. B., Yen, E. Y., & Valera, I. (2023) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2023-eular.683

Authors: Silkaitis, K., & Lemos, B.
Affiliations: Harvard University (US)
Corresponding author: Lemos, Bernardo
ORCID: Silkaitis, Katherine
Lemos, Bernardo
Venue: Biology of Sex Differences
Publisher: Springer Science and Business Media LLC
Published: 2014
Volume: 5
Issue: 1
Pages: 2
ISSN: 2042-6410 (ISSN-L)
DOI: 10.1186/2042-6410-5-2
PMC: PMC3907150
OpenAlex: W2129665448
Cited by: 39
References: 130
Citations by year: 2026: 1 · 2025: 1 · 2024: 2 · 2023: 5 · 2022: 5 · 2021: 2 · 2020: 2 · 2019: 5 · 2018: 2 · 2017: 6 · 2016: 7 · 2015: 1
FWCI: 3.07
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Biology of Sex Differences (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
Funders: Ellison Medical Foundation
National Heart, Lung, and Blood Institute (T32HL007118)
National Institute of General Medical Sciences (T34GM087239)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Keywords: sex differences, sex chromosomes, Y chromosome, autosomes, mitochondrial DNA, epigenetic regulation, sex-specific gene regulation, autoimmune disease, neurological disorders, testosterone, lupus, multiple sclerosis, gonadal differentiation, maternal inheritance

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Sex-biased chromatin and regulatory cross-talk between sex chromosomes, autosomes, and mitochondria

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