Human papillomavirus oncoproteins induce a reorganization of epithelial-associated γδ T cells promoting tumor formation

Proc Natl Acad Sci U S A. 2017 Oct 24;114(43):E9056-E9065. doi: 10.1073/pnas.1712883114. Epub 2017 Oct 10.

Abstract

It has been shown that γδ T cells protect against the formation of squamous cell carcinoma (SCC) in several models. However, the role of γδ T cells in human papillomavirus (HPV)-associated uterine cervical SCC, the third-leading cause of death by cancer in women, is unknown. Here, we investigated the impact of γδ T cells in a transgenic mouse model of carcinogenesis induced by HPV16 oncoproteins. Surprisingly, γδ T cells promoted the development of HPV16 oncoprotein-induced lesions. HPV16 oncoproteins induced a decrease in epidermal Skint1 expression and the associated antitumor Vγ5+ γδ T cells, which were replaced by γδ T-cell subsets (mainly Vγ6+ γδlowCCR2+CCR6-) actively producing IL-17A. Consistent with a proangiogenic role, γδ T cells promoted the formation of blood vessels in the dermis underlying the HPV-induced lesions. In human cervical biopsies, IL-17A+ γδ T cells could only be observed at the cancer stage (SCC), where HPV oncoproteins are highly expressed, supporting the clinical relevance of our observations in mice. Overall, our results suggest that HPV16 oncoproteins induce a reorganization of the local epithelial-associated γδ T-cell subpopulations, thereby promoting angiogenesis and cancer development.

Keywords: functional heterogeneity; gammadelta; interleukin 17; viral oncogene; γδ T cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cervix Uteri
  • Epidermis / pathology
  • Epidermis / virology
  • Female
  • Humans
  • Immunoglobulins / metabolism
  • Interleukin-17 / metabolism
  • Intraepithelial Lymphocytes / pathology*
  • Intraepithelial Lymphocytes / virology*
  • Mice, Transgenic
  • Neoplasms, Squamous Cell / pathology
  • Neoplasms, Squamous Cell / virology*
  • Neovascularization, Pathologic
  • Oncogene Proteins, Viral / metabolism
  • Papillomavirus E7 Proteins / metabolism
  • Papillomavirus Infections / pathology*
  • Papillomavirus Infections / virology
  • Receptors, CCR2 / metabolism
  • Receptors, CCR6 / metabolism
  • Repressor Proteins / metabolism
  • Uterine Cervical Neoplasms / pathology
  • Uterine Cervical Neoplasms / virology*

Substances

  • CCR6 protein, mouse
  • Ccr2 protein, mouse
  • E6 protein, Human papillomavirus type 16
  • IL17A protein, human
  • Immunoglobulins
  • Interleukin-17
  • Oncogene Proteins, Viral
  • Papillomavirus E7 Proteins
  • Receptors, CCR2
  • Receptors, CCR6
  • Repressor Proteins
  • Skint1 protein, mouse
  • oncogene protein E7, Human papillomavirus type 16