Role of interferon-γ and cytotoxic T lymphocytes in intraocular tumor rejection

J Leukoc Biol. 2016 May;99(5):735-47. doi: 10.1189/jlb.3A0315-093RRR. Epub 2015 Nov 17.

Abstract

The eye is normally an immunosuppressive environment. This condition is better known as immune privilege and protects the eye from immune-mediated inflammation of tissues that cannot regenerate. However, immune privilege creates a dilemma for the eye when intraocular neoplasms arise. In some cases, immune privilege is suspended, resulting in the immune rejection of intraocular tumors. This study employed a mouse model in which interferon-γ-dependent intraocular tumor rejection occurs. We tested the hypothesis that this rejection requires interferon-γ for the generation and functional capacity of cytotoxic T lymphocyte-mediated rejection of intraocular tumors. Tumors grew progressively in the eyes of interferon-γ knockout mice, even though the mice generated tumor-specific cytotoxic T lymphocyte responses in the periphery. However, interferon-γ knockout mice rejected tumors that were introduced into extraocular sites. Subcutaneous tumor immunization before intraocular challenge led to tumor rejection and preservation of the eye in wild-type mice. By contrast, tumors grew progressively in the eyes of interferon-γ knockout mice despite their ability to generate peripheral tumor-specific cytotoxic T lymphocytes as well as the capacity of CD8(+) T cells to enter the eye as shown by the presence of CD8 and perforin message and CD3(+)CD8(+) leukocytes within the tumor-bearing eye. We found that cytotoxic T lymphocytes generated in wild-type mice and adoptively transferred into interferon-γ knockout mice mediated the rejection of intraocular tumors in interferon-γ knockout hosts. The results indicate that interferon-γ is critical for the initial priming and differentiation of cytotoxic T lymphocytes residing in the periphery to produce the most effect antitumor function within the eye.

Keywords: CTL; IFN-γ; eye; immune privilege; necrotic inflammation.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • Adoptive Transfer
  • Animals
  • CD3 Complex / metabolism
  • CD4 Antigens / metabolism
  • CD8-Positive T-Lymphocytes / immunology
  • Cell Adhesion Molecules / metabolism
  • Cell Proliferation
  • Cytotoxicity, Immunologic
  • Eye Neoplasms / immunology*
  • Eye Neoplasms / pathology*
  • Immunization
  • Interferon-gamma / metabolism*
  • Mice, Inbred C57BL
  • Mice, Knockout
  • P-Selectin / metabolism
  • Perforin / metabolism
  • T-Lymphocytes, Cytotoxic / immunology*
  • T-Lymphocytes, Helper-Inducer / immunology

Substances

  • CD3 Complex
  • CD4 Antigens
  • Cell Adhesion Molecules
  • P-Selectin
  • Perforin
  • Interferon-gamma