The Y chromosome and its impact on health and disease (2024)

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The Y chromosome and its impact on health and disease (1)

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Hum Mol Genet. 2021 Oct 15; 30(R2): R296–R300.

Published online 2021 Jul 29. doi:10.1093/hmg/ddab215

PMCID: PMC8490013

PMID: 34328177

Melissa A Wilson

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The Y chromosome is the most gene-deficient chromosome in the human genome (though not the smallest chromosome) and has largely been sequestered away from large-scale studies of the effects of genetics on human health. Here I review the literature, focusing on the last 2 years, for recent evidence of the role of the Y chromosome in protecting from or contributing to disease. Although many studies have focused on Y chromosome gene copy number and variants in fertility, the role of the Y chromosome in human health is now known to extend too many other conditions including the development of multiple cancers and Alzheimer’s disease. I further include the discussion of current technology and methods for analyzing Y chromosome variation. The true role of the Y chromosome and associated genetic variants in human disease will only become clear when the Y chromosome is integrated into larger studies of human genetic variation, rather than being analyzed in isolation.

Introduction to Y Chromosome in Health and Disease

The human Y chromosome has a unique evolutionary history and an increasingly strong signal for a role in contributing to sex differences in health and disease via both direct genetic mechanisms and indirect regulation. A typical human genome will contain either two X chromosomes or an X and a Y chromosome. Although it is well-documented that the X chromosome plays an important role in human health and disease (reviewed in (1–3), among others), the X chromosome is often still excluded from human genetic and genomics analyses (4,5). That said, the X chromosome is still included in far more studies than the Y chromosome for which methods and technology lag even further behind. Given documented sex differences in aging (6), the immune system (7) and cancer (8) all possible underlying mechanisms should be investigated (Table 1). Here I will briefly introduce the anatomy of the human Y chromosome, discuss evidence focusing on the past 2 years for the role of Y-linked genes and sex chromosome dosage in human disease, and conclude with technological challenges and opportunities for growth in including the Y chromosome in future human genetics research.

Table 1

Sex chromosome variation affects human health. Variation on the human X and Y chromosomes can have significant effects on human health. It is important to keep in mind that although the Y chromosome is typically limited to people who develop testis, this is not always the case (e.g. Swyer syndrome, a condition where females have an X and a Y chromosome (35)), and all humans have at least one X chromosome. The X and Y chromosomes do not represent ‘female’ and ‘male’, but rather contain genes and regulatory elements that act independently of, or in addition to, the effects of gonadal hormones. This table describes some common sex chromosome variations and gives some examples of how those variations are related to human health

X chromosomeY chromosome
Whole or partial chromosome copy number variationCommon karyotypes: XX, XY, X0, XXY, XXX, XXXX.Common Karyotypes: XY, XYY, XXYY.
Gene dosageEpigenetic silencing of X-linked genesX-linked genes are equally likely to be hyper- and hypo-methylated with age (25).Epigenetic silencing of Y-linked genesY-linked genes are likely to be hyper-methylated with age (25).
Genes that are subject to or escape inactivation in individuals with 2 or more X chromosomesX-linked genes on the inactive X chromosome show variable patterns of escape from inactivation (36).Gene copy number variationDosage of genes in the azoospermia factor (AZF) regions are known to be important for fertility, including USP9Y, DBY, UTY, TBY4, DAZ, CDY1, and TSPY1 (37).
Somatic lossLoss of one X chromosome in individuals with two or more X chromosomesLoss of X chromosome increases with age in XX females (38).Loss of the Y chromosomeLoss of the Y chromosome is associated with increased risk of cancer, Alzheimer’s disease, and cardiovascular disease (17).
Gene mutationsAffect gene functionMutations in the X-linked KDM5C affect heart development in females and males (29).Affect gene functionThe Y-linked gene, UTY, when functional, reduces pro-inflammatory cytokines and endothelial cell death (28).

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Evolution and Anatomy of the Human Y Chromosome

We can better understand mechanisms of Y chromosome gene expression and regulation in human health and disease by first understanding its unique evolutionary history. The human Y and X chromosomes used to be entirely hom*ologous, meaning they shared the same gene content and same evolutionary origin (9). However, over millions of years, the human Y lost 90% of the genes it once shared with the X (10), but also gained genes via transposition and amplification (11). Because of this, the Y chromosome is not just a degenerated X chromosome. In fact, many Y chromosome genes evolve under strong purifying selection (12), some show signatures of positive selection (13) and Y-linked genes likely evolved unique functions and expression patterns critical for survival (14). Taking these signatures together suggests that the human Y chromosome gene content, whereas small relative to the rest of the genome, may nonetheless have a large impact on human health.

Loss of Y-linked Gene Content and Expression Implicated in Disease

Perhaps, the strongest signal of the importance for Y chromosome gene content in human health is research that focuses on the loss of Y-linked gene content and its consequences (Fig. 1). One of the largest areas of research regarding the loss of Y-linked gene content and human health revolves around gene copy number and fertility in sperm-producing XY individuals. Two recent reviews discuss the abundant evidence for how micro-deletions on the human Y chromosome are causal in infertility, affecting sperm development, motility and function. First, Punjani et al. (15) discuss how mutations on the Y chromosome are implicated in as many as 15% of cases of low (oligozoospermia) or absent (azoospermia) sperm count. Further, Signore et al. (16) similarly review the literature showing that Y chromosome structural rearrangements, whole chromosome copy number, and individual gene copy number may be important to explaining infertility in XY individuals who do not have a family history of infertility (idiopathic infertility).

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Figure 1

Mechanisms of Y chromosome affecting human health and disease. Typical genetic male cells will have one X chromosome (blue with stripes) and one Y chromosome (solid green). Although there are many genes that are unique to the X or Y chromosome, there are some that have a functional copy on both the X (e.g. UTX/KDM6A, shown here as a dark blue band) and the Y (e.g. UTY, dark green band) chromosomes. These genes will express transcripts (blue or green squiggles, respectively) in typical cells. In a bulk tissue sample, early in life, all of the cells will show expression from the Y chromosome (bottom left square). However, as individuals age, they can lose functionality of the Y in two main ways. First, their cells could start to lose the Y chromosome completely, a process called loss of Y, in which a portion of cells loses the Y chromosome during cell division and all daughter cells no longer have the Y chromosome at all (top right box). In this case, the proportion of cells in a bulk sample that exhibit loss of Y can range from 0 to 100%. The second primary way to lose functionality on the Y is for the genes to be methylated (or as happens on the Y chromosome with aging, hyper-methylated). In this case, the Y chromosome will still be present, but individual genes will be silenced via methylation (bottom left box). The approaches will be different for distinguishing these two mechanism of loss of Y functionality.

In addition to individual gene loss, there is mounting evidence that mosaic loss of the entire Y chromosome in adult (somatic) tissues may be important for disease development over time. Guo et al. (17) survey the literature on age-related loss of Y chromosomes and conclude that this loss is not a neutral process, as previously believed, but rather that this loss is associated with onset and severity of multiple diseases. The somatic loss of Y chromosomes from cells has been observed in bone marrow, being significantly associated with the diagnosis of abnormal growths (myeloid neoplasia) (18). Recently, partial or complete loss of the Y chromosome was reported to be strongly associated with reduced survival in Barrett’s adenocarcinoma, from a median overall survival of 58.8months with a complete Y chromosome to a reduced overall survival of 19.4months without (19). That said, in a study that tracked loss of Y chromosome in blood in patients across 22years, the loss of Y chromosomes in the blood was progressive in some patients, increasing over time, and static in others (20), suggesting that the proportion of a sample with the loss of Y chromosome alone may not be sufficient as a biomarker for the likelihood of disease.

Finally, although complete structural variation, loss and copy number variation have all been observed to be associated with disease, it may be sufficient just to have a reduction in Y-linked gene expression for effects on health to be observed. An analysis of 47 non-diseased tissues from the Genotype Tissue EXpression project and 12 cancer types from The Cancer Genome Atlas concluded that the loss of Y chromosome gene expression was associated with cancer risk, with an odds ratio of 3.66 (21). The same group also reported that in an analysis of gene expression from cases of patients with Alzheimer’s disease and controls, there was both decreased expression of Y-linked genes with age, and that this was more common in patients with Alzheimer’s disease (22). One potential mechanism may be age-related methylation changes. Notably, there is a 2020 patent to use methylation on the Y chromosome as a biomarker for early and rapid prostate cancer diagnosis, with higher levels of methylation being prognostic for prostate cancer (23). Curiously, and perhaps in contrast to the overall gene expression result mentioned above and prognostic methylation patent, an analysis of CpG methylation in blood from 624 patients from four cohorts reported opposite patterns of age-related methylation on autosomes compared with the Y chromosome (24); although autosomal methylation tended to decrease with age, Y-linked methylation tended to increase, but importantly, the authors reported that hypermethylation on the Y chromosome is associated with reduced risk of death. Another study that focused on the X and Y chromosome also reported the propensity for Y-linked methylation to trend toward hypermethylation with age, whereas X-linked methylation showed approximately equal levels of hyper- and hypo-methylation with age (25), similar to the autosomes. Future work will need to reconcile these findings.

X-Y hom*ologous Genes Are Not Identical in Function

When thinking about potential mechanism of genes regulating human health, there has been a lot of attention paid to the role of sex-linked genes and the immune system. In particular, X-linked genes and their expression in individuals with two X chromosomes is strongly implicated in autoimmunity, as well as potentially being protective against viral infections (reviewed in (26)). However, a recent study reported that the X chromosome actually has fewer total immune system-related genes than autosomes, whereas when ranking gene function, immune system-related genes were the second most prominent category on the Y chromosome (27). About half of the single copy genes on the Y chromosome have a functional copy on the X because of their shared evolutionary origin, but it seems that often the Y-linked and X-linked copies have diverged in function. Recently, it was reported that one of these Y-linked genes, UTY, functions to reduce both pro-inflammatory cytokines and endothelial cell death, which are protective against the lung disease pulmonary hypertension (28). Further, careful studies of the X-liked and Y-linked hom*ologs KDM5C and KDM5D show that the two genes are important for heart development and have conserved function. All individuals with a mutated X-linked version of the gene have challenges with heart development, but XY individuals can be missing either the X-linked or the Y-linked copy and so long as their existing copy does not have any mutations these individuals will not develop heart malformations (specifically non-compaction cardiomyopathy) (29).

Methodological and Technical Advances to Incorporating the Y Chromosome in Genetic Analyses

There are several technical challenges to incorporating the Y chromosome into studies of human health and disease, some of which can now be addressed with advances in methodology and technology. The reason that analysis of DNA and RNA is particularly challenging on the Y chromosomes is that it shares sequence hom*ology and similarity with the X chromosome, and other parts of the genome. Thus, sequencing reads can mis-map between the sex chromosomes. Unfortunately, although new methodological approaches have been suggested to improve DNA sequence alignment (30), and RNA sequence mapping (31) on the sex chromosomes, these have primarily focused on improving quantification of reads on the X chromosome and not the Y chromosome.

One way to get a better handle on Y-linked sequences is to focus sequencing efforts on just this region of the genome. To work toward this, Yano et al. (32) in a mouse model used a fluorescence-activated cell sorter (FACS) in conjunction with ultraviolet and blue 488nm lasers to sort the DNA in M-phase sells and size-select to enrich their DNA sample for Y chromosomes. This sorting does not exclusively select Y chromosomes, here also selecting 5 other non-sex chromosomes with approximately equal or higher proportion. Following FACS selection, the entire set was sequenced with long-read Oxford Nanopore MinION sequencing, with a total of 6.59% of the sequencing reads mapping to the Y chromosome (32). The researchers then de novo assembled and analyzed the mouse Y chromosome from these data. Although this approach has the benefit of improving the quality of the DNA sequence analysis on the Y chromosome, and measuring unique variants there, it requires additional approaches that are not always available for a given sample (e.g. the preparation of M-phase cells may not be feasible with all samples), and equipment that is not as readily available as the sequencing technology (e.g. FACS machines and lasers are less accessible to a general laboratory than the MinION or other sequencing technologies).

If one is less interested in specific Y-chromosome variants, and rather seeking to measure the proportion of cells in a sample that have lost the Y chromosome (also called loss of Y or LOY), there are additional approaches. Recent work from Danielsson et al. (20) tested three different approaches for measuring LOY in bulk tissue samples—genotyping array, whole genome sequencing, and their newly proposed ddPCR of a 6bp region of the AMELY and AMELX genes—finding that there was high agreement between them. This bodes well for reanalyzing the ever-growing number of human samples available that have previously been processed with genotype arrays or whole genome sequencing.

Future Directions

Future work to identify and understand the role of the Y chromosome in human health and disease processes will take a shift in the way human genetics treats the Y chromosome. Most of the recent articles published here focus exclusively on the Y chromosome and its role in health and disease, whether focusing on the LOY or loss of gene expression via hypermethylation. But rarely is the Y chromosome incorporated alongside the rest of the genome. Given that genetic background—the suite of genetic mutations interacting together—can have as large of an interacting effect on disease as age and sex (33), it is not sufficient to study the Y chromosome in isolation. Similarly, the Y chromosome and its variants may have a significant role on autosomal gene expression. Evidence from flies suggests that the Y chromosome may affect autosomal gene expression via shaping patterns of heterochromatin genome-wide (34). It will be important to determine whether the Y chromosome similarly affects heterochromatin across the human genome.


This study was supported by the National Institute of General Medical Sciences of the National Institutes of Health under Award Number R35GM124827 to MAW. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.


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The Y chromosome and its impact on health and disease (2024)


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