MYCN controls an alternative RNA splicing program in high-risk metastatic neuroblastoma

Cancer Lett. 2016 Feb 28;371(2):214-24. doi: 10.1016/j.canlet.2015.11.045. Epub 2015 Dec 10.

Abstract

The molecular mechanisms underlying the aggressive behavior of MYCN driven neuroblastoma (NBL) is under intense investigation; however, little is known about the impact of this family of transcription factors on the splicing program. Here we used high-throughput RNA sequencing to systematically study the expression of RNA isoforms in stage 4 MYCN-amplified NBL, an aggressive subtype of metastatic NBL. We show that MYCN-amplified NBL tumors display a distinct gene splicing pattern affecting multiple cancer hallmark functions. Six splicing factors displayed unique differential expression patterns in MYCN-amplified tumors and cell lines, and the binding motifs for some of these splicing factors are significantly enriched in differentially-spliced genes. Direct binding of MYCN to promoter regions of the splicing factors PTBP1 and HNRNPA1 detected by ChIP-seq demonstrates that MYCN controls the splicing pattern by direct regulation of the expression of these key splicing factors. Furthermore, high expression of PTBP1 and HNRNPA1 was significantly associated with poor overall survival of stage4 NBL patients (p ≤ 0.05). Knocking down PTBP1, HNRNPA1 and their downstream target PKM2, an isoform of pro-tumor-growth, result in repressed growth of NBL cells. Therefore, our study reveals a novel role of MYCN in controlling global splicing program through regulation of splicing factors in addition to its well-known role in the transcription program. These findings suggest a therapeutically potential to target the key splicing factors or gene isoforms in high-risk NBL with MYCN-amplification.

Keywords: MYCN-amplification; Neuroblastoma; RNA isoforms; RNA-seq; Splicing.

MeSH terms

  • Alternative Splicing*
  • Binding Sites
  • Biomarkers, Tumor / genetics*
  • Biomarkers, Tumor / metabolism
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cell Line, Tumor
  • Cell Proliferation
  • Chromatin Immunoprecipitation
  • Gene Amplification
  • Gene Expression Regulation, Neoplastic
  • Heterogeneous Nuclear Ribonucleoprotein A1
  • Heterogeneous-Nuclear Ribonucleoprotein Group A-B / genetics
  • Heterogeneous-Nuclear Ribonucleoprotein Group A-B / metabolism
  • Heterogeneous-Nuclear Ribonucleoproteins / genetics
  • Heterogeneous-Nuclear Ribonucleoproteins / metabolism
  • High-Throughput Nucleotide Sequencing
  • Humans
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • N-Myc Proto-Oncogene Protein
  • Neoplasm Staging
  • Neuroblastoma / genetics*
  • Neuroblastoma / metabolism
  • Neuroblastoma / mortality
  • Nuclear Proteins / genetics*
  • Nuclear Proteins / metabolism
  • Oncogene Proteins / genetics*
  • Oncogene Proteins / metabolism
  • Polypyrimidine Tract-Binding Protein / genetics
  • Polypyrimidine Tract-Binding Protein / metabolism
  • Promoter Regions, Genetic
  • RNA Interference
  • RNA, Neoplasm / genetics*
  • RNA, Neoplasm / metabolism
  • Risk Factors
  • Thyroid Hormone-Binding Proteins
  • Thyroid Hormones / genetics
  • Thyroid Hormones / metabolism
  • Transcription, Genetic
  • Transfection

Substances

  • Biomarkers, Tumor
  • Carrier Proteins
  • Heterogeneous Nuclear Ribonucleoprotein A1
  • Heterogeneous-Nuclear Ribonucleoprotein Group A-B
  • Heterogeneous-Nuclear Ribonucleoproteins
  • MYCN protein, human
  • Membrane Proteins
  • N-Myc Proto-Oncogene Protein
  • Nuclear Proteins
  • Oncogene Proteins
  • PTBP1 protein, human
  • RNA, Neoplasm
  • Thyroid Hormones
  • hnRNPA1 protein, human
  • Polypyrimidine Tract-Binding Protein