HDAC6 inhibition induces glioma stem cells differentiation and enhances cellular radiation sensitivity through the SHH/Gli1 signaling pathway

Cancer Lett. 2018 Feb 28:415:164-176. doi: 10.1016/j.canlet.2017.12.005. Epub 2017 Dec 6.

Abstract

The existence of small numbers of stem-like cells, called glioma stem cells (GSCs), in human glioblastoma multiforme (GBM) is responsible for recurrence due to resistance to radiotherapy and chemotherapy. Inhibition of histone deacetylase 6 (HDAC6) enhanced radiosensitivity of cancer cells. However, the effect of inhibiting HDAC6 on stemness and radioresistance of GSCs and its molecular mechanism are largely unknown. In the present study, we found that HDAC6 was upregulated in GSCs comparing to non-stem tumor cells. Inhibiting HDAC6 downregulated glioma-associated oncogene homolog 1 (Gli1), Patched (Ptch1 and Ptch2) receptors, components of SHH signal, expression and activity in GSCs. Restraining HDAC6 decreased cell proliferation, induces differentiation and increased apoptosis of GSCs via inactivation of SHH/Gli1 signaling pathway. Moreover, HDAC6 inhibition decreased DNA damage repair capacity of GSCs through degradation of checkpoint kinase (CHK) 1 caused by X-linked inhibitor of apoptosis (XIAP) downregulation, leading to elevated radiosensitivity. Taken together, these findings indicate that HDAC6 inhibition decreased stemness of GSCs and enhanced GSCs radiosensitivity through inactivating SHH/Gli1 pathway. This provides a promising novel drug target to overcome GSCs stemness and radioresistance.

Keywords: Gli1; Gloima stem cells; HDAC6; Hedgehog pathway; Radioresistance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain Neoplasms / genetics*
  • Brain Neoplasms / metabolism
  • Brain Neoplasms / therapy
  • Cell Differentiation / genetics*
  • Cell Differentiation / radiation effects
  • Cell Line, Tumor
  • Gene Expression Regulation, Neoplastic
  • Glioblastoma / genetics*
  • Glioblastoma / metabolism
  • Glioblastoma / therapy
  • Hedgehog Proteins / genetics*
  • Hedgehog Proteins / metabolism
  • Histone Deacetylase 6 / genetics*
  • Histone Deacetylase 6 / metabolism
  • Humans
  • Kaplan-Meier Estimate
  • Male
  • Mice, Nude
  • Neoplastic Stem Cells / metabolism*
  • Neoplastic Stem Cells / radiation effects
  • RNA Interference
  • RNAi Therapeutics / methods
  • Signal Transduction / genetics
  • Signal Transduction / radiation effects
  • Xenograft Model Antitumor Assays / methods
  • Zinc Finger Protein GLI1 / genetics*
  • Zinc Finger Protein GLI1 / metabolism

Substances

  • GLI1 protein, human
  • Hedgehog Proteins
  • SHH protein, human
  • Zinc Finger Protein GLI1
  • HDAC6 protein, human
  • Histone Deacetylase 6