Induction of tumor cell apoptosis in vivo increases tumor antigen cross-presentation, cross-priming rather than cross-tolerizing host tumor-specific CD8 T cells

J Immunol. 2003 May 15;170(10):4905-13. doi: 10.4049/jimmunol.170.10.4905.

Abstract

Cross-presentation of cell-bound Ags from established, solid tumors to CD8 cells is efficient and likely to have a role in determining host response to tumor. A number of investigators have predicted that when tumor Ags are derived from apoptotic cells either no response, due to Ag "sequestration," or CD8 cross-tolerance would ensue. Because the crucial issue of whether this happens in vivo has never been addressed, we induced apoptosis of established hemagglutinin (HA)-transfected AB1 tumors in BALB/c mice using the apoptosis-inducing reagent gemcitabine. This shrank the tumor by approximately 80%. This induction of apoptosis increased cross-presentation of HA to CD8 cells yet neither gross deletion nor functional tolerance of HA-specific CD8 cells were observed, based on tetramer analysis, proliferation of specific CD8 T cells, and in vivo CTL activity. Interestingly, apoptosis primed the host for a strong antitumor response to a second, virus-generated HA-specific signal in that administration of an HA-expressing virus after gemcitabine administration markedly decreased tumor growth compared with viral administration without gemcitabine. Thus tumor cell apoptosis in vivo neither sequesters tumor Ags nor cross-tolerizes tumor-specific CD8 cells. This observation has fundamental consequences for the development of tumor immunotherapy protocols and for understanding T cell reactivity to tumors and the in vivo immune responses to apoptotic cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigen Presentation* / drug effects
  • Antigen-Presenting Cells / immunology
  • Antigen-Presenting Cells / metabolism
  • Antigens, Neoplasm / immunology*
  • Antigens, Neoplasm / metabolism
  • Apoptosis / drug effects
  • Apoptosis / immunology*
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / metabolism
  • Clonal Anergy / drug effects
  • Clonal Anergy / immunology*
  • Clonal Deletion / drug effects
  • Clonal Deletion / immunology
  • Cytotoxicity, Immunologic / drug effects
  • Deoxycytidine / administration & dosage
  • Deoxycytidine / analogs & derivatives*
  • Dose-Response Relationship, Immunologic
  • Epitopes, T-Lymphocyte / immunology
  • Epitopes, T-Lymphocyte / metabolism
  • Gemcitabine
  • Growth Inhibitors / administration & dosage
  • Hemagglutinin Glycoproteins, Influenza Virus / immunology
  • Hemagglutinin Glycoproteins, Influenza Virus / metabolism
  • Immunization
  • Injections, Intraperitoneal
  • Mesothelioma / drug therapy
  • Mesothelioma / immunology*
  • Mesothelioma / pathology*
  • Mesothelioma / prevention & control
  • Mice
  • Mice, Inbred BALB C
  • Mice, Transgenic
  • Tumor Cells, Cultured
  • Up-Regulation / drug effects
  • Up-Regulation / immunology*

Substances

  • Antigens, Neoplasm
  • Epitopes, T-Lymphocyte
  • Growth Inhibitors
  • Hemagglutinin Glycoproteins, Influenza Virus
  • Deoxycytidine
  • Gemcitabine