Epigenomic and transcriptomic signatures of a 47,XXY karyotype in the brain

Joana Viana1,*, Ruth Pidsley2,3,*, Claire Troakes2, Helen Spiers2, Chloe C. Y. Wong2, Safa Al-Sarraj2, Ian Craig2, Leonard Schalkwyk2, Jonathan Mill1,2,^

* These authors contributed equally

^ Corresponding author

1 University of Exeter Medical School, Exeter University, UK

2 Institute of Psychiatry, King¿s College London, UK

3 Garvan Institute of Medical Research, Sydney 2010, Australia

Klinefelter's syndrome (KS) is the most common sex-chromosome aneuploidy in humans. Most affected individuals carry one extra X-chromosome (karyotype 47,XXY) and the condition presents with a heterogeneous mix of reproductive, physical and psychiatric phenotypes. Although the mechanism(s) by which the supernumerary X-chromosome determines these features of KS are poorly understood, skewed X-chromosome inactivation (XCI), gene-dosage dysregulation, and the parental origin of the extra X-chromosome have all been implicated suggesting an important role for epigenetic processes. During the standard quality control procedures of an integrated -omics study of schizophrenia we identified an individual with a 47,XXY karyotype. This subject was comorbid for schizophrenia and had a notably reduced cerebellum mass compared to other individuals in the study (n=49). Using post-mortem prefrontal cortex and cerebellum tissue we assessed methylomic and transcriptomic changes in this individual relative to samples with wild-type 46,XX or 46,XY karyotypes. Numerous locus-specific changes in DNA methylation and gene expression were observed, with many differences being autosomal and tissue-specific. Global DNA methylation, assessed via the interrogation of LINE-1 and Alu repetitive elements, was significantly altered in the 47,XXY subject in a tissue-specific manner with extreme global DNA hypomethylation detected in the prefrontal cortex and extreme global DNA hypermethylation in the cerebellum. This study provides the first detailed molecular characterization of the prefrontal cortex and cerebellum from an individual with karyotype 47,XXY, identifying widespread tissue-specific epigenomic and transcriptomic alterations in the brain.

Supplemental files

Track files created using the Integrative Genomics Viewer software, which can be download from http://www.broadinstitute.org/igv/ .

DNA methylation data of genes escaping X-chromosome inactivation in the cerebellum of a 47,XXY individual compared to 46,XY males and 46,XX females

IGV track file 1.igv

DNA methylation data of genes escaping X-chromosome inactivation in the prefrontal cortex of a 47,XXY individual compared to 46,XY males and 46,XX females

IGV track file 2.igv

Gene expression data of genes escaping X-chromosome inactivation in the cerebellum of a 47,XXY individual compared to 46,XY males and 46,XX females

IGV track file 3.igv

Gene expression data of genes escaping X-chromosome inactivation in the prefrontal cortex of a 47,XXY individual compared to 46,XY males and 46,XX females

IGV track file 4.igv