MYCN and HIF-1 directly regulate TET1 expression to control 5-hmC gains and enhance neuroblastoma cell migration in hypoxia

Epigenetics. 2022 Dec;17(13):2056-2074. doi: 10.1080/15592294.2022.2106078. Epub 2022 Aug 8.

Abstract

Ten-Eleven-Translocation 5-methylcytosine dioxygenases 1-3 (TET1-3) convert 5-methylcytosine to 5-hydroxymethylcytosine (5-hmC), using oxygen as a co-substrate. Contrary to expectations, hypoxia induces 5-hmC gains in MYCN-amplified neuroblastoma (NB) cells via upregulation of TET1. Here, we show that MYCN directly controls TET1 expression in normoxia, and in hypoxia, HIF-1 augments TET1 expression and TET1 protein stability. Through gene-editing, we identify two MYCN and HIF-1 binding sites within TET1 that regulate gene expression. Bioinformatic analyses of 5-hmC distribution and RNA-sequencing data from hypoxic cells implicate hypoxia-regulated genes important for cell migration, including CXCR4. We show that hypoxic cells lacking the two MYCN/HIF-1 binding sites within TET1 migrate slower than controls. Treatment of MYCN-amplified NB cells with a CXCR4 antagonist results in slower migration under hypoxic conditions, suggesting that inclusion of a CXCR4 antagonist into NB treatment regimens could be beneficial for children with MYCN-amplified NBs.

Keywords: MYCN; TET1; hypoxia; neuroblastoma.

Plain language summary

In MYCN-amplified neuroblastoma cell lines, MYCN directly controls TET1 expression in normoxia.In MYCN-amplified neuroblastoma cell lines exposed to hypoxia, HIF-1 augments TET1 expression and TET1 protein stability.Hypoxic MYCN-amplified neuroblastoma cell lines have increased cell migration, mediated by genes including CXCR4 that gain 5-hydroxymethylcytosine density.Treatment of MYCN-amplified NB cells with a CXCR4 antagonist slows hypoxia-associated migration, suggesting a CXCR4 antagonist could be beneficial in treatment regimens for children with MYCN-amplified neuroblastomas.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • 5-Methylcytosine* / metabolism
  • Cell Hypoxia / genetics
  • Cell Line, Tumor
  • Cell Movement
  • DNA Methylation
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Hypoxia / genetics
  • Hypoxia-Inducible Factor 1* / genetics
  • Hypoxia-Inducible Factor 1* / metabolism
  • Mixed Function Oxygenases* / genetics
  • Mixed Function Oxygenases* / metabolism
  • N-Myc Proto-Oncogene Protein* / genetics
  • N-Myc Proto-Oncogene Protein* / metabolism
  • Neuroblastoma* / genetics
  • Neuroblastoma* / metabolism
  • Proto-Oncogene Proteins* / genetics
  • Proto-Oncogene Proteins* / metabolism

Substances

  • 5-Methylcytosine
  • Mixed Function Oxygenases
  • MYCN protein, human
  • N-Myc Proto-Oncogene Protein
  • Proto-Oncogene Proteins
  • TET1 protein, human
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1