Local immunosuppression induced by high viral load of human papillomavirus: characterization of cellular phenotypes producing interleukin-10 in cervical neoplastic lesions

Immunology. 2015 Sep;146(1):113-21. doi: 10.1111/imm.12487. Epub 2015 Jul 1.

Abstract

A specific immune response to human papillomavirus (HPV) in the cervical microenvironment plays a key role in eradicating infection and eliminating mutated cells. However, high-risk HPVs modulate immune cells to create an immunosuppressive microenvironment, and induce these immune cells to produce interleukin 10 (IL-10). This production of IL-10, in conjunction with HPV infection, contributes to the appearance of cervical neoplastic lesions. We sought to characterize the IL-10-producing cellular phenotype, and investigate the influence of host and HPV factors upon the induction of an immunosuppressive microenvironment. Immunohistochemical analysis demonstrated an increase in IL-10 production by keratinocytes, macrophages and Langerhans cells in high-grade cervical lesions and cervical cancer. This increase was more pronounced in patients older than 30 years, and was also correlated with high viral load, and infection with a single HPV type, particularly high-risk HPVs. Our results indicate the existence of a highly immunosuppressive microenvironment composed of different IL-10-producing cellular phenotypes in cervical cancer samples, and samples classified as high-grade cervical lesions (cervical intraepithelial neoplasia stages II and III). The immunosuppressive microenvironment that developed for these different cellular phenotypes favours viral persistence and neoplastic progression.

Keywords: human papillomavirus; immunosuppression; interleukin-10.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Aging
  • Female
  • Human papillomavirus 16 / immunology
  • Human papillomavirus 18 / immunology
  • Humans
  • Immune Tolerance / immunology*
  • Interleukin-10 / biosynthesis*
  • Interleukin-10 / immunology
  • Keratinocytes / metabolism
  • Langerhans Cells / metabolism
  • Macrophages / metabolism
  • Middle Aged
  • Papillomavirus Infections / immunology*
  • Papillomavirus Infections / virology
  • Tumor Microenvironment / immunology
  • Uterine Cervical Dysplasia / immunology*
  • Uterine Cervical Dysplasia / virology
  • Uterine Cervical Neoplasms / immunology*
  • Uterine Cervical Neoplasms / virology
  • Viral Load
  • Young Adult

Substances

  • IL10 protein, human
  • Interleukin-10