Long Noncoding RNA SChLAP1 Forms a Growth-Promoting Complex with HNRNPL in Human Glioblastoma through Stabilization of ACTN4 and Activation of NF-κB Signaling

Clin Cancer Res. 2019 Nov 15;25(22):6868-6881. doi: 10.1158/1078-0432.CCR-19-0747. Epub 2019 Sep 6.

Abstract

Purpose: Long noncoding RNAs (lncRNA) have essential roles in diverse cellular processes, both in normal and diseased cell types, and thus have emerged as potential therapeutic targets. A specific member of this family, the SWI/SNF complex antagonist associated with prostate cancer 1 (SChLAP1), has been shown to promote aggressive prostate cancer growth by antagonizing the SWI/SNF complex and therefore serves as a biomarker for poor prognosis. Here, we investigated whether SChLAP1 plays a potential role in the development of human glioblastoma (GBM).

Experimental design: RNA-ISH and IHC were performed on a tissue microarray to assess expression of SChLAP1 and associated proteins in human gliomas. Proteins complexed with SChLAP1 were identified using RNA pull-down and mass spectrometry. Lentiviral constructs were used for functional analysis in vitro and in vivo.

Results: SChLAP1 was increased in primary GBM samples and cell lines, and knockdown of the lncRNA suppressed growth. SChLAP1 was found to bind heterogeneous nuclear ribonucleoprotein L (HNRNPL), which stabilized the lncRNA and led to an enhanced interaction with the protein actinin alpha 4 (ACTN4). ACTN4 was also highly expressed in primary GBM samples and was associated with poorer overall survival in glioma patients. The SChLAP1-HNRNPL complex led to stabilization of ACTN4 through suppression of proteasomal degradation, which resulted in increased nuclear localization of the p65 subunit of NF-κB and activation of NF-κB signaling, a pathway associated with cancer development.

Conclusions: Our results implicated SChLAP1 as a driver of GBM growth as well as a potential therapeutic target in treatment of the disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actinin / metabolism*
  • Animals
  • Biomarkers, Tumor
  • Cell Line, Tumor
  • Cell Proliferation / genetics
  • Disease Models, Animal
  • Gene Expression Regulation, Neoplastic
  • Glioblastoma / genetics*
  • Glioblastoma / metabolism*
  • Glioblastoma / mortality
  • Glioblastoma / pathology
  • Humans
  • Mice
  • NF-kappa B / metabolism*
  • Prognosis
  • Proteasome Endopeptidase Complex / metabolism
  • Protein Binding
  • Protein Transport
  • Proteolysis
  • RNA, Long Noncoding / chemistry
  • RNA, Long Noncoding / genetics*
  • Ribonucleoproteins / metabolism*
  • Signal Transduction*
  • Ubiquitination
  • Xenograft Model Antitumor Assays

Substances

  • ACTN4 protein, human
  • Biomarkers, Tumor
  • HNRNPL protein, human
  • NF-kappa B
  • RNA, Long Noncoding
  • Ribonucleoproteins
  • SChLAP1 long noncoding RNA
  • Actinin
  • Proteasome Endopeptidase Complex