H3K27me3-mediated PGC1α gene silencing promotes melanoma invasion through WNT5A and YAP

J Clin Invest. 2020 Feb 3;130(2):853-862. doi: 10.1172/JCI130038.

Abstract

Oncogene-targeted and immune checkpoint therapies have revolutionized the clinical management of malignant melanoma and now offer hope to patients with advanced disease. Intimately connected to patients' overall clinical risk is whether the initial primary melanoma lesion will metastasize and cause advanced disease, but underlying mechanisms are not entirely understood. A subset of melanomas display heightened peroxisome proliferator-activated receptor γ coactivator 1-α (PGC1α) expression that maintains cell survival cues by promoting mitochondrial function, but also suppresses metastatic spread. Here, we show that PGC1α expression in melanoma cells was silenced by chromatin modifications that involve promoter H3K27 trimethylation. Pharmacological EZH2 inhibition diminished H3K27me3 histone markers, increased PGC1α expression, and functionally suppressed invasion within PGC1α-silenced melanoma cells. Mechanistically, PGC1α silencing activated transcription factor 12 (TCF12), to increase expression of WNT5A, which in turn stabilized YAP protein levels to promote melanoma migration and metastasis. Accordingly, inhibition of components of this transcription-signaling axis, including TCF12, WNT5A, or YAP, blocked melanoma migration in vitro and metastasis in vivo. These results indicate that epigenetic control of melanoma metastasis involved altered expression of PGC1α and an association with the inherent metabolic state of the tumor.

Keywords: Cancer; Cell Biology; Cell migration/adhesion; Melanoma; Oncology.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Animals
  • Basic Helix-Loop-Helix Transcription Factors
  • Cell Line, Tumor
  • Gene Expression Regulation, Neoplastic*
  • Gene Silencing*
  • HEK293 Cells
  • Histones / genetics
  • Histones / metabolism*
  • Humans
  • Melanoma, Experimental / genetics
  • Melanoma, Experimental / metabolism*
  • Melanoma, Experimental / pathology
  • Mice
  • Mice, Nude
  • Neoplasm Invasiveness
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha / biosynthesis*
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha / genetics
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Wnt-5a Protein / genetics
  • Wnt-5a Protein / metabolism*
  • YAP-Signaling Proteins

Substances

  • Adaptor Proteins, Signal Transducing
  • Basic Helix-Loop-Helix Transcription Factors
  • Histones
  • PPARGC1A protein, human
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Transcription Factors
  • WNT5A protein, human
  • Wnt-5a Protein
  • YAP-Signaling Proteins
  • YAP1 protein, human
  • TCF12 protein, human