Integrative Modeling Reveals Annexin A2-mediated Epigenetic Control of Mesenchymal Glioblastoma

EBioMedicine. 2016 Oct:12:72-85. doi: 10.1016/j.ebiom.2016.08.050. Epub 2016 Sep 18.

Abstract

Glioblastomas are characterized by transcriptionally distinct subtypes, but despite possible clinical relevance, their regulation remains poorly understood. The commonly used molecular classification systems for GBM all identify a subtype with high expression of mesenchymal marker transcripts, strongly associated with invasive growth. We used a comprehensive data-driven network modeling technique (augmented sparse inverse covariance selection, aSICS) to define separate genomic, epigenetic, and transcriptional regulators of glioblastoma subtypes. Our model identified Annexin A2 (ANXA2) as a novel methylation-controlled positive regulator of the mesenchymal subtype. Subsequent evaluation in two independent cohorts established ANXA2 expression as a prognostic factor that is dependent on ANXA2 promoter methylation. ANXA2 knockdown in primary glioblastoma stem cell-like cultures suppressed known mesenchymal master regulators, and abrogated cell proliferation and invasion. Our results place ANXA2 at the apex of a regulatory cascade that determines glioblastoma mesenchymal transformation and validate aSICS as a general methodology to uncover regulators of cancer subtypes.

Keywords: Annexin A2; Brain tumor stem cells; Data integration; Epigenetic regulation; Glioblastoma; Master regulators of cancer cell phenotypes; Mesenchymal transformation; New methods for integrative data analysis; Partial correlation based networks; Spare inverse covariance selection.

MeSH terms

  • Algorithms
  • Annexin A2 / genetics
  • Annexin A2 / metabolism*
  • Biomarkers, Tumor
  • Cell Line, Tumor
  • Computational Biology / methods
  • DNA Methylation
  • Databases, Nucleic Acid
  • Epigenesis, Genetic*
  • Epithelial-Mesenchymal Transition
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic*
  • Gene Knockdown Techniques
  • Glioblastoma / genetics*
  • Glioblastoma / metabolism*
  • Glioblastoma / mortality
  • Glioblastoma / pathology
  • Humans
  • Mesenchymoma / genetics*
  • Mesenchymoma / metabolism*
  • Mesenchymoma / mortality
  • Mesenchymoma / pathology
  • Molecular Sequence Annotation
  • Neoplasm Grading
  • Neoplastic Stem Cells / metabolism
  • Prognosis
  • Promoter Regions, Genetic

Substances

  • Annexin A2
  • Biomarkers, Tumor