Enhanced IL-6/IL-6R signaling promotes growth and malignant properties in EBV-infected premalignant and cancerous nasopharyngeal epithelial cells

PLoS One. 2013 May 1;8(5):e62284. doi: 10.1371/journal.pone.0062284. Print 2013.

Abstract

Nasopharyngeal carcinoma (NPC) is etiologically associated with Epstein-Barr virus (EBV) infection. However, the exact role of EBV in NPC pathogenesis remains elusive. Activation of signal transducer and activator of transcription 3 (STAT3) is common in human cancers including NPC and plays an important role in the pathogenesis and progression of human cancers. Interleukin-6 (IL-6), a major inflammatory cytokine, is a potent activator of STAT3. In this study, we report that EBV-infected immortalized nasopharyngeal epithelial (NPE) cells often acquire an enhanced response to IL-6-induced STAT3 activation to promote their growth and invasive properties. Interestingly, this enhanced IL-6/STAT3 response was mediated by overexpression of IL-6 receptor (IL-6R). Furthermore, IL-6R overexpression enhanced IL-6-induced STAT3 activation in uninfected immortalized NPE cells in vitro, and promoted growth and tumorigenicity of EBV-positive NPC cell line (C666-1) in vivo. Moreover, it is shown for the first time that IL-6R was overexpressed in clinical specimens of NPC. IL-6 expression could also be strongly detected in the stromal cells of NPC and a higher circulating level of IL-6 was found in the sera of advance-staged NPC patients compared to the control subjects. Therefore, IL-6R overexpression, coupled with enhanced IL-6/STAT3 signaling may facilitate the malignant transformation of EBV-infected premalignant NPE cells into cancer cells, and enhance malignant properties of NPC cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Cell Proliferation
  • Epithelial Cells / physiology*
  • Epstein-Barr Virus Infections / immunology
  • Epstein-Barr Virus Infections / metabolism*
  • Gene Expression
  • Gene Expression Regulation, Neoplastic
  • Herpesvirus 4, Human / immunology*
  • Humans
  • Interleukin-6 / genetics
  • Interleukin-6 / metabolism*
  • Male
  • Mice
  • Mice, Nude
  • Nasopharyngeal Neoplasms / metabolism*
  • Nasopharyngeal Neoplasms / pathology
  • Nasopharyngeal Neoplasms / virology
  • Neoplasm Transplantation
  • Precancerous Conditions / metabolism*
  • Precancerous Conditions / pathology
  • Precancerous Conditions / virology
  • Receptors, Interleukin-6 / metabolism*
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction
  • Tumor Burden
  • Up-Regulation
  • Viral Matrix Proteins / genetics
  • Viral Matrix Proteins / metabolism

Substances

  • EBV-associated membrane antigen, Epstein-Barr virus
  • IL6 protein, human
  • Interleukin-6
  • Receptors, Interleukin-6
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Viral Matrix Proteins