Radiation Sensitization of Basal Cell and Head and Neck Squamous Cell Carcinoma by the Hedgehog Pathway Inhibitor Vismodegib

Int J Mol Sci. 2018 Aug 23;19(9):2485. doi: 10.3390/ijms19092485.

Abstract

Vismodegib, an inhibitor of the Hedgehog signaling pathway, is an approved drug for monotherapy in locally advanced or metastatic basal cell carcinoma (BCC). Data on combined modality treatment by vismodegib and radiation therapy, however, are rare. In the present study, we examined the radiation sensitizing effects of vismodegib by analyzing viability, cell cycle distribution, cell death, DNA damage repair and clonogenic survival in three-dimensional cultures of a BCC and a head and neck squamous cell carcinoma (HNSCC) cell line. We found that vismodegib decreases expression of the Hedgehog target genes glioma-associated oncogene homologue (GLI1) and the inhibitor of apoptosis protein (IAP) Survivin in a cell line- and irradiation-dependent manner, most pronounced in squamous cell carcinoma (SCC) cells. Furthermore, vismodegib significantly reduced proliferation in both cell lines, while additional irradiation only slightly further impacted on viability. Analyses of cell cycle distribution and cell death induction indicated a G1 arrest in BCC and a G2 arrest in HNSCC cells and an increased fraction of cells in SubG1 phase following combined treatment. Moreover, a significant rise in the number of phosphorylated histone-2AX/p53-binding protein 1 (γH2AX/53BP1) foci in vismodegib- and radiation-treated cells was associated with a significant radiosensitization of both cell lines. In summary, these findings indicate that inhibition of the Hedgehog signaling pathway may increase cellular radiation response in BCC and HNSCC cells.

Keywords: basal cell carcinoma; head and neck squamous cell carcinoma; hedgehog signaling pathway; radiotherapy resistance; vismodegib (GDC-0449).

MeSH terms

  • Anilides / pharmacology*
  • Antineoplastic Agents / pharmacology*
  • Carcinoma, Basal Cell / genetics
  • Carcinoma, Basal Cell / metabolism
  • Carcinoma, Basal Cell / pathology
  • Carcinoma, Basal Cell / therapy
  • Carcinoma, Squamous Cell / genetics
  • Carcinoma, Squamous Cell / metabolism
  • Carcinoma, Squamous Cell / pathology
  • Carcinoma, Squamous Cell / therapy
  • Cell Line, Tumor
  • Combined Modality Therapy / methods
  • G1 Phase Cell Cycle Checkpoints / drug effects
  • G1 Phase Cell Cycle Checkpoints / radiation effects
  • G2 Phase Cell Cycle Checkpoints / drug effects
  • G2 Phase Cell Cycle Checkpoints / radiation effects
  • Gamma Rays / therapeutic use*
  • Gene Expression Regulation, Neoplastic*
  • Head and Neck Neoplasms / genetics
  • Head and Neck Neoplasms / metabolism
  • Head and Neck Neoplasms / pathology
  • Head and Neck Neoplasms / therapy
  • Hedgehog Proteins / antagonists & inhibitors*
  • Hedgehog Proteins / genetics
  • Hedgehog Proteins / metabolism
  • Histones / genetics
  • Histones / metabolism
  • Humans
  • Organ Specificity
  • Pyridines / pharmacology*
  • Radiation-Sensitizing Agents / pharmacology*
  • Signal Transduction
  • Skin Neoplasms / genetics
  • Skin Neoplasms / metabolism
  • Skin Neoplasms / pathology
  • Skin Neoplasms / therapy
  • Survivin / genetics
  • Survivin / metabolism
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism
  • Zinc Finger Protein GLI1 / genetics
  • Zinc Finger Protein GLI1 / metabolism

Substances

  • Anilides
  • Antineoplastic Agents
  • BIRC5 protein, human
  • GLI1 protein, human
  • H2AX protein, human
  • Hedgehog Proteins
  • HhAntag691
  • Histones
  • Pyridines
  • Radiation-Sensitizing Agents
  • Survivin
  • Tumor Suppressor Protein p53
  • Zinc Finger Protein GLI1