TWIST1-WDR5- Hottip Regulates Hoxa9 Chromatin to Facilitate Prostate Cancer Metastasis

Cancer Res. 2017 Jun 15;77(12):3181-3193. doi: 10.1158/0008-5472.CAN-16-2797. Epub 2017 May 8.

Abstract

TWIST1 is a transcription factor critical for development that can promote prostate cancer metastasis. During embryonic development, TWIST1 and HOXA9 are coexpressed in mouse prostate and then silenced postnatally. Here we report that TWIST1 and HOXA9 coexpression are reactivated in mouse and human primary prostate tumors and are further enriched in human metastases, correlating with survival. TWIST1 formed a complex with WDR5 and the lncRNA Hottip/HOTTIP, members of the MLL/COMPASS-like H3K4 methylases, which regulate chromatin in the Hox/HOX cluster during development. TWIST1 overexpression led to coenrichment of TWIST1 and WDR5 as well as increased H3K4me3 chromatin at the Hoxa9/HOXA9 promoter, which was dependent on WDR5. Expression of WDR5 and Hottip/HOTTIP was also required for TWIST1-induced upregulation of HOXA9 and aggressive cellular phenotypes such as invasion and migration. Pharmacologic inhibition of HOXA9 prevented TWIST1-induced aggressive prostate cancer cellular phenotypes in vitro and metastasis in vivo This study demonstrates a novel mechanism by which TWIST1 regulates chromatin and gene expression by cooperating with the COMPASS-like complex to increase H3K4 trimethylation at target gene promoters. Our findings highlight a TWIST1-HOXA9 embryonic prostate developmental program that is reactivated during prostate cancer metastasis and is therapeutically targetable. Cancer Res; 77(12); 3181-93. ©2017 AACR.

MeSH terms

  • Animals
  • Blotting, Western
  • Cell Line, Tumor
  • Chromatin
  • Fluorescent Antibody Technique
  • Gene Expression Regulation, Neoplastic / genetics
  • Gene Knockout Techniques
  • Heterografts
  • Histone-Lysine N-Methyltransferase / genetics
  • Histone-Lysine N-Methyltransferase / metabolism*
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism*
  • Humans
  • Immunohistochemistry
  • Immunoprecipitation
  • Intracellular Signaling Peptides and Proteins
  • Male
  • Mice
  • Neoplasm Invasiveness / genetics*
  • Neoplasm Invasiveness / pathology
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Polymerase Chain Reaction
  • Prostatic Neoplasms / genetics
  • Prostatic Neoplasms / pathology*
  • RNA, Long Noncoding / genetics
  • RNA, Long Noncoding / metabolism*
  • Twist-Related Protein 1 / genetics
  • Twist-Related Protein 1 / metabolism*

Substances

  • Chromatin
  • Homeodomain Proteins
  • Intracellular Signaling Peptides and Proteins
  • Nuclear Proteins
  • RNA, Long Noncoding
  • TWIST1 protein, human
  • Twist-Related Protein 1
  • WDR5 protein, human
  • homeobox protein HOXA9
  • long noncoding RNA HOTTIP, human
  • Histone-Lysine N-Methyltransferase