Critical role of indoleamine 2,3-dioxygenase in tumor resistance to repeated treatments with targeted IFNgamma

Mol Cancer Ther. 2008 Dec;7(12):3859-66. doi: 10.1158/1535-7163.MCT-08-0538.

Abstract

Targeted delivery of IFNgamma to tumors has been achieved by fusing this cytokine with GCNGRC, a tumor neovasculature homing peptide. Although the therapeutic efficacy of this protein (called IFNgamma-NGR) in animal models is greater than that of IFNgamma, frequent administrations of IFNgamma-NGR may result in lower efficacy and tumor resistance. We investigated the role of indoleamine 2,3-dioxygenase (IDO), an IFNgamma-inducible enzyme that may down-regulate T cells by affecting local tryptophan catabolism in tumor resistance to repeated treatments with IFNgamma-NGR. The study was carried out in immunocompetent mice and in nu/nu mice bearing RMA lymphoma, B16F melanoma, or WEHI-164 fibrosarcoma and in vitro using cultured tumor cells. IDO activity was increased in lymphoma homogenates after multiple treatments with IFNgamma-NGR but not after a single treatment. Coadministration of 1-methyl-tryptophan, an inhibitor of IDO, increased tumor responses to multiple treatments in the lymphoma, melanoma, and fibrosarcoma models. No synergism between IFNgamma-NGR and 1-methyl-tryptophan was observed in vitro in tumor cell proliferation assays or in nu/nu tumor-bearing mice, suggesting that the antitumor effect was host mediated. We conclude that IDO is critically involved in tumor resistance to repeated treatments with IFNgamma-NGR, likely causing excessive stimulation of tryptophan catabolism and inhibiting antitumor immune mechanisms. Coadministration of IFNgamma-NGR with IDO inhibitors could represent a new strategy for increasing its antitumor activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology*
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm*
  • Gene Expression Regulation, Neoplastic*
  • Humans
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / pharmacology*
  • Interferon-gamma / metabolism
  • Interferon-gamma / physiology*
  • Melanoma, Experimental
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Nude
  • Neoplasms / drug therapy*
  • Neoplasms / pathology
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / pharmacology*
  • Tryptophan / analogs & derivatives
  • Tryptophan / pharmacology

Substances

  • Antineoplastic Agents
  • IFNgamma-NGR peptide
  • Indoleamine-Pyrrole 2,3,-Dioxygenase
  • Recombinant Fusion Proteins
  • Interferon-gamma
  • Tryptophan