BET inhibitor suppresses melanoma progression via the noncanonical NF-κB/SPP1 pathway

Theranostics. 2020 Sep 15;10(25):11428-11443. doi: 10.7150/thno.47432. eCollection 2020.

Abstract

Background: Bromodomain and extra-terminal domain (BET) inhibitors have shown profound efficacy against hematologic malignancies and solid tumors in preclinical studies. However, the underlying molecular mechanism in melanoma is not well understood. Here we identified secreted phosphoprotein 1 (SPP1) as a melanoma driver and a crucial target of BET inhibitors in melanoma. Methods: Bioinformatics analysis and meta-analysis were used to evaluate the SPP1 expression in normal tissues, primary melanoma, and metastatic melanoma. Real-time PCR (RT-PCR) and Western blotting were employed to quantify SPP1 expression in melanoma cells and tissues. Cell proliferation, wound healing, and Transwell assays were carried out to evaluate the effects of SPP1 and BET inhibitors in melanoma cells in vitro. A xenograft mouse model was used to investigate the effect of SPP1 and BET inhibitors on melanoma in vivo. Chromatin immunoprecipitation (ChIP) assay was performed to evaluate the regulatory mechanism of BET inhibitors on SPP1. Results: SPP1 was identified as a melanoma driver by bioinformatics analysis, and meta-analysis determined it to be a diagnostic and prognostic biomarker for melanoma. SPP1 overexpression was associated with poor melanoma prognosis, and silencing SPP1 suppressed melanoma cell proliferation, migration, and invasion. Through a pilot drug screen, we identified BET inhibitors as ideal therapeutic agents that suppressed SPP1 expression. Also, SPP1 overexpression could partially reverse the suppressive effect of BET inhibitors on melanoma. We further demonstrated that bromodomain-containing 4 (BRD4) regulated SPP1 expression. Notably, BRD4 did not bind directly to the SPP1 promoter but regulated SPP1 expression through NFKB2. Silencing of NFKB2 resembled the phenotype of BET inhibitors treatment and SPP1 silencing in melanoma. Conclusion: Our findings highlight SPP1 as an essential target of BET inhibitors and provide a novel mechanism by which BET inhibitors suppress melanoma progression via the noncanonical NF-κB/SPP1 pathway.

Keywords: BET inhibitor; SPP1; melanoma.; noncanonical NF-κB pathway.

Publication types

  • Meta-Analysis
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology*
  • Antineoplastic Agents / therapeutic use
  • Biomarkers, Tumor / antagonists & inhibitors
  • Biomarkers, Tumor / genetics
  • Biomarkers, Tumor / metabolism
  • Cell Cycle Proteins / antagonists & inhibitors*
  • Cell Cycle Proteins / metabolism
  • Cell Line, Tumor
  • Cell Movement / drug effects
  • Cell Movement / genetics
  • Cell Proliferation / genetics
  • Chemotherapy, Adjuvant / methods
  • Computational Biology
  • Datasets as Topic
  • Disease Progression
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects
  • Gene Expression Regulation, Neoplastic / genetics
  • Gene Knockdown Techniques
  • HEK293 Cells
  • Humans
  • Male
  • Melanoma / genetics
  • Melanoma / mortality
  • Melanoma / secondary
  • Melanoma / therapy*
  • Mice
  • Middle Aged
  • NF-kappa B p52 Subunit / genetics
  • NF-kappa B p52 Subunit / metabolism
  • Neoplasm Invasiveness / genetics
  • Neoplasm Invasiveness / prevention & control
  • Osteopontin / antagonists & inhibitors
  • Osteopontin / genetics*
  • Osteopontin / metabolism
  • Prognosis
  • Promoter Regions, Genetic
  • RNA-Seq
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Skin / pathology
  • Skin Neoplasms / genetics
  • Skin Neoplasms / mortality
  • Skin Neoplasms / pathology
  • Skin Neoplasms / therapy*
  • Transcription Factors / antagonists & inhibitors*
  • Transcription Factors / metabolism
  • Up-Regulation
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents
  • BRD4 protein, human
  • Biomarkers, Tumor
  • Cell Cycle Proteins
  • NF-kappa B p52 Subunit
  • NFKB2 protein, human
  • SPP1 protein, human
  • Transcription Factors
  • Osteopontin