The homeoprotein HOXB2 limits triple-negative breast carcinogenesis via extracellular matrix remodeling

Int J Biol Sci. 2024 Jan 20;20(3):1045-1063. doi: 10.7150/ijbs.88837. eCollection 2024.

Abstract

Homeobox genes and their encoded DNA-binding homeoproteins are master regulators of development. Consequently, these homeotic elements may regulate key steps in cancer pathogenesis. Here, using a combination of in silico analyses of large-scale patient datasets, in vitro RNAi phenotyping, and in vivo validation studies, we investigated the role of HOXB2 in different molecular subtypes of human breast cancer (BC). The gene expression signatures of HOXB2 are different across distinct BC subtypes due to various genetic alterations, but HOXB2 was specifically downregulated in the aggressive triple-negative subtype (TNBC). We found that the reduced expression of HOXB2 was correlated with the metastatic abilities (epithelial-to-mesenchymal transition) of TNBC cells. Further, we revealed that HOXB2 restrained TNBC aggressiveness by ECM organization. HOXB2 bound to the promoter regions of MATN3 and ECM2 and regulated their transcription levels. Forced expression of HOXB2 effectively prevented TNBC progression and metastasis in a mouse xenograft model. Reduction of HOXB2 and the HOXB2/MATN3/ECM2 transcriptional axis correlated with poor survival in patients with various cancers. Further, we found the long non-coding RNA HOXB-AS1 in complex with SMYD3, a lysine methyltransferase, as an epigenetic switch controlling HOXB2 expression. Overall, our results indicate a tumor-suppressive role of HOXB2 by maintaining ECM organization and delineate potential clinical utility of HOXB2 as a marker for TNBC patients.

Keywords: ECM; EMT; HOXB2; cancer metastasis; triple-negative breast cancer.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Cell Movement
  • Cell Proliferation / genetics
  • Cell Transformation, Neoplastic / genetics
  • Epithelial-Mesenchymal Transition / genetics
  • Extracellular Matrix / metabolism
  • Gene Expression Regulation, Neoplastic
  • Genes, Homeobox
  • Histone-Lysine N-Methyltransferase / genetics
  • Homeodomain Proteins* / genetics
  • Humans
  • Mice
  • Transcription Factors* / genetics
  • Triple Negative Breast Neoplasms* / metabolism

Substances

  • Histone-Lysine N-Methyltransferase
  • Homeodomain Proteins
  • HOXB2 protein, human
  • SMYD3 protein, human
  • Transcription Factors