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CTCF haploinsufficiency destabilizes DNA methylation and predisposes to cancer
Christopher J Kemp1, James M Moore1, Russell Moser1
1Division of Human Biology, Fred Hutchinson Cancer Research Center, Seattle, WA 98109, USA.
Abstract:
Epigenetic alterations, particularly in DNA methylation, are ubiquitous in cancer, yet the molecular origins and the consequences of these alterations are poorly understood. CTCF, a DNA-binding protein that regulates higher-order chromatin organization, is frequently altered by hemizygous deletion or mutation in human cancer. To date, a causal role for CTCF in cancer has not been established. Here, we show that Ctcf hemizygous knockout mice are markedly susceptible to spontaneous, radiation-, and chemically induced cancer in a broad range of tissues. Ctcf(+/-) tumors are characterized by increased aggressiveness, including invasion, metastatic dissemination, and mixed epithelial/mesenchymal differentiation. Molecular analysis of Ctcf(+/-) tumors indicates that Ctcf is haploinsufficient for tumor suppression. Tissues with hemizygous loss of CTCF exhibit increased variability in CpG methylation genome wide. These findings establish CTCF as a prominent tumor-suppressor gene and point to CTCF-mediated epigenetic stability as a major barrier to neoplastic progression.
Insights
CTCF loss causes cancer. Hemizygous loss of CTCF leads to increased cancer susceptibility and aggressiveness by disrupting epigenetic stability, establishing CTCF as a tumor suppressor.
Area of Science:
- Cancer Biology
- Epigenetics
- Genomics
Background:
- Epigenetic alterations, especially DNA methylation changes, are common in cancer but their origins and effects are unclear.
- CTCF, a chromatin organizer, is often altered in human cancers, but its causal role in tumorigenesis remains unproven.
Purpose of the Study:
- To investigate the role of CTCF in cancer development and tumor suppression.
- To determine if CTCF haploinsufficiency contributes to cancer susceptibility and epigenetic instability.
Main Methods:
- Generation and analysis of Ctcf hemizygous knockout (Ctcf(+/-)) mice.
- Assessment of tumor incidence, aggressiveness (invasion, metastasis), and differentiation in Ctcf(+/-) mice.
- Genome-wide CpG methylation analysis in tissues with hemizygous CTCF loss.
Main Results:
- Ctcf(+/-) mice showed high susceptibility to spontaneous, radiation-, and chemically induced cancers across various tissues.
- Tumors from Ctcf(+/-) mice exhibited increased aggressiveness, invasion, metastasis, and mixed epithelial/mesenchymal features.
- Hemizygous loss of CTCF resulted in widespread variability in CpG methylation across the genome.
Conclusions:
- CTCF is a critical tumor suppressor, and its haploinsufficiency promotes cancer development.
- CTCF plays a vital role in maintaining epigenetic stability, acting as a barrier against neoplastic progression.
- Disruption of CTCF function leads to genome-wide methylation instability, contributing to cancer aggressiveness.
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