DNA methylation profiling identifies two splenic marginal zone lymphoma subgroups with different clinical and genetic features

Blood. 2015 Mar 19;125(12):1922-31. doi: 10.1182/blood-2014-08-596247. Epub 2015 Jan 22.

Abstract

Splenic marginal zone lymphoma is a rare lymphoma. Loss of 7q31 and somatic mutations affecting the NOTCH2 and KLF2 genes are the commonest genomic aberrations. Epigenetic changes can be pharmacologically reverted; therefore, identification of groups of patients with specific epigenomic alterations might have therapeutic relevance. Here we integrated genome-wide DNA-promoter methylation profiling with gene expression profiling, and clinical and biological variables. An unsupervised clustering analysis of a test series of 98 samples identified 2 clusters with different degrees of promoter methylation. The cluster comprising samples with higher-promoter methylation (High-M) had a poorer overall survival compared with the lower (Low-M) cluster. The prognostic relevance of the High-M phenotype was confirmed in an independent validation set of 36 patients. In the whole series, the High-M phenotype was associated with IGHV1-02 usage, mutations of NOTCH2 gene, 7q31-32 loss, and histologic transformation. In the High-M set, a number of tumor-suppressor genes were methylated and repressed. PRC2 subunit genes and several prosurvival lymphoma genes were unmethylated and overexpressed. A model based on the methylation of 3 genes (CACNB2, HTRA1, KLF4) identified a poorer-outcome patient subset. Exposure of splenic marginal zone lymphoma cell lines to a demethylating agent caused partial reversion of the High-M phenotype and inhibition of proliferation.

Publication types

  • Multicenter Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Cell Proliferation
  • Cell Transformation, Neoplastic
  • Cluster Analysis
  • DNA Methylation*
  • DNA Mutational Analysis
  • Female
  • Gene Expression Profiling
  • Humans
  • Kaplan-Meier Estimate
  • Kruppel-Like Factor 4
  • Lymphoma, B-Cell, Marginal Zone / diagnosis
  • Lymphoma, B-Cell, Marginal Zone / genetics*
  • Lymphoma, B-Cell, Marginal Zone / mortality
  • Male
  • Middle Aged
  • Mutation
  • Phenotype
  • Prognosis
  • Promoter Regions, Genetic
  • Splenic Neoplasms / diagnosis
  • Splenic Neoplasms / genetics*
  • Splenic Neoplasms / mortality
  • Treatment Outcome