M2 macrophages reduce the radiosensitivity of head and neck cancer by releasing HB‑EGF

Oncol Rep. 2020 Aug;44(2):698-710. doi: 10.3892/or.2020.7628. Epub 2020 May 29.

Abstract

The aim of the present study was to examine the potential role of human heparin‑binding epidermal growth factor (HB‑EGF) secreted by M2 macrophages in the development of radioresistance in head and neck squamous cell carcinoma (HNSCC). Immunohistochemistry was used to detect radiosensitivity in human papilloma virus (HPV)‑positive and HPV‑negative HNSCC tissues and immunohistochemical staining with specific antibodies for macrophage surface markers was used to assess the infiltration of M1 and M2 macrophages in HPV‑positive and ‑negative HNSCC tissues. The expression of HB‑EGF in HPV‑positive and ‑negative HNSCC tissues was determined by multi‑cytokine detection in order to determine the relationship between HB‑EGF and radiosensitivity. M1 and M2 macrophages were co‑cultured with the HNSCC cell line CAL27 and treated with HB‑EGF and its neutralizing antibodies to assess radiation sensitivity. Finally, the major DNA double‑strand break repair pathways required for the activation of HB‑EGF and promotion of epidermal growth factor receptor (EGFR) were identified. The results revealed that radiosensitivity was higher in HPV‑positive HNSCC compared with HPV‑negative. There was a higher infiltration of M2 macrophages in HPV‑negative HNSCC, which were revealed as the main source of HB‑EGF secretion. Furthermore, it was determined that overexpression of HB‑EGF induced radioresistance in HPV‑negative HNSCC. HB‑EGF promoted the activation of the non‑homologous end‑joining pathway by activating EGFR. To the best of our knowledge, this is the first study to demonstrate the association between HB‑EGF and radiosensitivity in HNSCC. These results indicated that the secretion of HB‑EGF by M2 macrophages could induce radioresistance of HPV‑negative HNSCC.

Keywords: head and neck squamous cell carcinoma; human papillomavirus; radiosensitivity; M2 macrophages; heparin-binding epidermal growth factor.

MeSH terms

  • Cell Line, Tumor
  • Coculture Techniques
  • DNA Breaks, Double-Stranded / radiation effects
  • DNA End-Joining Repair
  • ErbB Receptors / metabolism
  • Female
  • Head and Neck Neoplasms / immunology
  • Head and Neck Neoplasms / pathology
  • Head and Neck Neoplasms / radiotherapy*
  • Head and Neck Neoplasms / virology
  • Heparin-binding EGF-like Growth Factor / metabolism*
  • Humans
  • Macrophages / immunology*
  • Macrophages / metabolism
  • Male
  • Middle Aged
  • Papillomaviridae / isolation & purification
  • Papillomavirus Infections / immunology
  • Papillomavirus Infections / pathology
  • Papillomavirus Infections / radiotherapy*
  • Papillomavirus Infections / virology
  • Radiation Tolerance / immunology*
  • Squamous Cell Carcinoma of Head and Neck / immunology
  • Squamous Cell Carcinoma of Head and Neck / pathology
  • Squamous Cell Carcinoma of Head and Neck / radiotherapy*
  • Squamous Cell Carcinoma of Head and Neck / virology

Substances

  • HBEGF protein, human
  • Heparin-binding EGF-like Growth Factor
  • EGFR protein, human
  • ErbB Receptors