Enduring epigenetic landmarks define the cancer microenvironment

Author:

Pidsley Ruth,Lawrence Mitchell G.,Zotenko Elena,Niranjan Birunthi,Statham Aaron,Song Jenny,Chabanon Roman M.,Qu Wenjia,Wang Hong,Richards Michelle,Nair Shalima S.,Armstrong Nicola J.,Nim Hieu T.,Papargiris Melissa,Balanathan Preetika,French Hugh,Peters Timothy,Norden Sam,Ryan Andrew,Pedersen John,Kench James,Daly Roger J.,Horvath Lisa G.,Stricker Phillip,Frydenberg Mark,Taylor Renea A.,Stirzaker Clare,Risbridger Gail P.,Clark Susan J.

Abstract

The growth and progression of solid tumors involves dynamic cross-talk between cancer epithelium and the surrounding microenvironment. To date, molecular profiling has largely been restricted to the epithelial component of tumors; therefore, features underpinning the persistent protumorigenic phenotype of the tumor microenvironment are unknown. Using whole-genome bisulfite sequencing, we show for the first time that cancer-associated fibroblasts (CAFs) from localized prostate cancer display remarkably distinct and enduring genome-wide changes in DNA methylation, significantly at enhancers and promoters, compared to nonmalignant prostate fibroblasts (NPFs). Differentially methylated regions associated with changes in gene expression have cancer-related functions and accurately distinguish CAFs from NPFs. Remarkably, a subset of changes is shared with prostate cancer epithelial cells, revealing the new concept of tumor-specific epigenome modifications in the tumor and its microenvironment. The distinct methylome of CAFs provides a novel epigenetic hallmark of the cancer microenvironment and promises new biomarkers to improve interpretation of diagnostic samples.

Funder

Cancer Australia

National Health and Medical Research Council

Cancer Institute of New South Wales

Australian Prostate Cancer Research Centre-NSW

Prostate Cancer Foundation of Australia

Movember Young Investigator

Victorian Cancer Agency

RT Hall Trust

TissuPath Pathology

Publisher

Cold Spring Harbor Laboratory

Subject

Genetics (clinical),Genetics

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