IL-17 suppresses immune effector functions in human papillomavirus-associated epithelial hyperplasia

J Immunol. 2014 Sep 1;193(5):2248-57. doi: 10.4049/jimmunol.1400216. Epub 2014 Jul 25.

Abstract

Persistent infection with high-risk human papillomaviruses (HPV) causes epithelial hyperplasia that can progress to cancer and is thought to depend on immunosuppressive mechanisms that prevent viral clearance by the host. IL-17 is a cytokine with diverse functions in host defense and in the pathology of autoimmune disorders, chronic inflammatory diseases, and cancer. We analyzed biopsies from patients with HPV-associated cervical intraepithelial neoplasia grade 2/3 and murine skin displaying HPV16 E7 protein-induced epithelial hyperplasia, which closely models hyperplasia in chronic HPV lesions. Expression of IL-17 and IL-23, a major inducer of IL-17, was elevated in both human HPV-infected and murine E7-expressing lesions. Using a skin-grafting model, we demonstrated that IL-17 in HPV16 E7 transgenic skin grafts inhibited effective host immune responses against the graft. IL-17 was produced by CD3(+) T cells, predominantly CD4(+) T cells in human, and CD4(+) and γδ T cells in mouse hyperplastic lesions. IL-23 and IL-1β, but not IL-18, induced IL-17 production in E7 transgenic skin. Together, these findings demonstrate an immunosuppressive role for IL-17 in HPV-associated epithelial hyperplasia and suggest that blocking IL-17 in persistent viral infection may promote antiviral immunity and prevent progression to cancer.

Publication types

  • Clinical Trial
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • CD4-Positive T-Lymphocytes
  • Female
  • Human papillomavirus 16 / genetics
  • Human papillomavirus 16 / immunology*
  • Humans
  • Interleukin-17 / immunology*
  • Interleukin-1beta / genetics
  • Interleukin-1beta / immunology
  • Interleukin-23 / genetics
  • Interleukin-23 / immunology
  • Mice
  • Mice, Knockout
  • Papillomavirus E7 Proteins / genetics
  • Papillomavirus E7 Proteins / immunology*
  • Papillomavirus Infections / genetics
  • Papillomavirus Infections / immunology*
  • Papillomavirus Infections / pathology
  • Receptors, Antigen, T-Cell, gamma-delta / genetics
  • Receptors, Antigen, T-Cell, gamma-delta / immunology
  • Uterine Cervical Dysplasia / genetics
  • Uterine Cervical Dysplasia / immunology*
  • Uterine Cervical Dysplasia / pathology
  • Uterine Cervical Neoplasms / genetics
  • Uterine Cervical Neoplasms / immunology*
  • Uterine Cervical Neoplasms / pathology

Substances

  • IL1B protein, human
  • IL1B protein, mouse
  • Interleukin-17
  • Interleukin-1beta
  • Interleukin-23
  • Papillomavirus E7 Proteins
  • Receptors, Antigen, T-Cell, gamma-delta
  • oncogene protein E7, Human papillomavirus type 16