Colorectal cancer (CRC) typically develops from intraepithelial neoplasms known as adenomas. Genomic profiling of these premalignant lesions presents an opportunity to discover molecular changes that can lead to colorectal cancer. Some of the earliest changes are epigenetic, including hypermethylation of the promoters of tumour suppressor genes. To identify such changes we performed whole genome DNA methylation profiling (MBD-Seq) on fifteen large adenomas and matched normal mucosa. We then validated epigenetic changes in a cohort of 105 adenomas using Combined Bisulfite Restriction Analysis (COBRA), bisulphite sequencing and quantitative(Q) RT-PCR. This approach identified the deubiquitinase USP44 as a gene that is frequently inactivated by DNA methylation.
Analysis of MBD-seq data identified the CpG island promoter of USP44 was methylated in 11/15 adenomas. In the larger cohort, USP44 was methylated in ~80% of 105 adenomas, but in only 10% of 48 matched normal mucosa. USP44 was also methylated in 100% of 18 CRC cell lines. Q RT-PCR showed that hypermethylation of USP44 correlated with a decrease in expression in 6/8 adenomas. Treatment of four CRC cell lines with the DNA demethylating agent 5-Aza-2'-deoxycytidine (5azaDC) resulted in a 10-250 fold increase in expression. We confirmed ectopic expression of USP44 in HEK293T cells caused a global depletion of H2BK120ub as measured by western blotting. This epigenetic mark is distributed throughout the transcribed region of active genes and is required for gene activation and transcriptional elongation. We are generating stable cell lines with USP44 knock-down and will present data on the global and site-specific effects on H2BK120ub levels following USP44 depletion.
In summary, we show that epigenetic inactivation of the deubiquitinase USP44 is a frequent and early event in colorectal adenomas. We propose changes in H2BK120ub arise from the epigenetic inactivation of USP44, which contributes to colorectal carcinogenesis through changes in gene expression across the genome.