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Clinical and Developmental Immunology
Volume 2012 (2012), Article ID 173029, 12 pages
http://dx.doi.org/10.1155/2012/173029
Research Article

Immunological and Nonimmunological Effects of Indoleamine 2,3-Dioxygenase on Breast Tumor Growth and Spontaneous Metastasis Formation

1Department of Medicine, University of Pittsburgh Cancer Institute, Pittsburgh, PA 15213, USA
2University of Pittsburgh Cancer Institute, Hillman Cancer Center, Pittsburgh, PA 15213, USA
3Department of Immunology, University of Pittsburgh Cancer Institute, Pittsburgh, PA 15213, USA
4Department of Pathology, University of Pittsburgh Cancer Institute, Pittsburgh, PA 15213, USA

Received 27 January 2012; Accepted 6 March 2012

Academic Editor: Masoud H. Manjili

Copyright © 2012 Vera Levina et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. Hanahan and R. A. Weinberg, “Hallmarks of cancer: the next generation,” Cell, vol. 144, no. 5, pp. 646–674, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. R. Kim, M. Emi, and K. Tanabe, “Cancer immunoediting from immune surveillance to immune escape,” Immunology, vol. 121, no. 1, pp. 1–14, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. T. Raskovalova, A. Lokshin, X. Huang et al., “Inhibition of cytokine production and cytotoxic activity of human antimelanoma specific CD8+ and CD4+ T lymphocytes by adenosine-protein kinase A type I signaling,” Cancer Research, vol. 67, no. 12, pp. 5949–5956, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. Y. Su, E. K. Jackson, and E. Gorelik, “Receptor desensitization and blockade of the suppressive effects of prostaglandin E2and adenosine on the cytotoxic activity of human melanoma-infiltrating T lymphocytes,” Cancer Immunology, Immunotherapy, vol. 60, no. 1, pp. 111–122, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. A. J. Muller, J. B. DuHadaway, P. S. Donover, E. Sutanto-Ward, and G. C. Prendergast, “Inhibition of indoleamine 2,3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy,” Nature Medicine, vol. 11, no. 3, pp. 312–319, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. A. J. Muller, W. P. Malachowski, and G. C. Prendergast, “Indoleamine 2,3-dioxygenase in cancer: targeting pathological immune tolerance with small-molecule inhibitors,” Expert Opinion on Therapeutic Targets, vol. 9, no. 4, pp. 831–849, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. D. H. Munn, “Indoleamine 2,3-dioxygenase, tumor-induced tolerance and counter-regulation,” Current Opinion in Immunology, vol. 18, no. 2, pp. 220–225, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. D. H. Munn and A. L. Mellor, “Indoleamine 2,3-dioxygenase and tumor-induced tolerance,” Journal of Clinical Investigation, vol. 117, no. 5, pp. 1147–1154, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. D. H. Munn and A. L. Mellor, “IDO and tolerance to tumors,” Trends in Molecular Medicine, vol. 10, no. 1, pp. 15–18, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. Y. Kudo and C. A. R. Boyd, “Human placental indoleamine 2,3-dioxygenase: cellular localization and characterization of an enzyme preventing fetal rejection,” Biochimica et Biophysica Acta, vol. 1500, no. 1, pp. 119–124, 2000. View at Publisher · View at Google Scholar · View at Scopus
  11. A. L. Mellor and D. H. Munn, “Tryptophan catabolism and T-cell tolerance: immunosuppression by starvation?” Immunology Today, vol. 20, no. 10, pp. 469–473, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. D. H. Munn, E. Shafizadeh, J. T. Attwood, I. Bondarev, A. Pashine, and A. L. Mellor, “Inhibition of T cell proliferation by macrophage tryptophan catabolism,” Journal of Experimental Medicine, vol. 189, no. 9, pp. 1363–1372, 1999. View at Publisher · View at Google Scholar · View at Scopus
  13. G. C. Prendergast, “Immune escape as a fundamental trait of cancer: focus on IDO,” Oncogene, vol. 27, no. 28, pp. 3889–3900, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. G. C. Prendergast, R. Metz, and A. J. Muller, “IDO recruits Tregs in melanoma,” Cell Cycle, vol. 8, no. 12, pp. 1818–1819, 2009. View at Scopus
  15. R. Yoshida and O. Hayaishi, “Induction of pulmonary indoleamine 2,3-dioxygenase by intraperitoneal injection of bacterial lipopolysaccharide,” Proceedings of the National Academy of Sciences of the United States of America, vol. 75, no. 8, pp. 3998–4000, 1978. View at Scopus
  16. R. Yoshida, J. Imanishi, and T. Oku, “Induction of pulmonary indoleamine 2,3-dioxygenase by interferon,” Proceedings of the National Academy of Sciences of the United States of America, vol. 78, no. 1, pp. 129–132, 1981. View at Scopus
  17. S. Lob, A. Königsrainer, H. G. Rammensee, G. Opelz, and P. Terness, “Inhibitors of indoleamine-2,3-dioxygenase for cancer therapy: can we see the wood for the trees?” Nature Reviews Cancer, vol. 9, no. 6, pp. 445–452, 2009. View at Scopus
  18. D. H. Munn, M. Zhou, J. T. Attwood et al., “Prevention of allogeneic fetal rejection by tryptophan catabolism,” Science, vol. 281, no. 5380, pp. 1191–1193, 1998. View at Scopus
  19. L. Huang, B. Baban, B. A. Johnson, and A. L. Mellor, “Dendritic cells, indoleamine 2,3 dioxygenase and acquired immune privilege,” International Reviews of Immunology, vol. 29, no. 2, pp. 133–155, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. P. Ligam, U. Manuelpillai, E. M. Wallace, and D. Walker, “Localisation of indoleamine 2,3-dioxygenase and kynurenine hydroxylase in the human placenta and decidua: implications for role of the kynurenine pathway in pregnancy,” Placenta, vol. 26, no. 6, pp. 498–504, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. N. Miwa, S. Hayakawa, S. Miyazaki et al., “IDO expression on decidual and peripheral blood dendritic cells and monocytes/macrophages after treatment with CTLA-4 or interferon-γ increase in normal pregnancy but decrease in spontaneous abortion,” Molecular Human Reproduction, vol. 11, no. 12, pp. 865–870, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. C. Uyttenhove, L. Pilotte, I. Théate et al., “Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase,” Nature Medicine, vol. 9, no. 10, pp. 1269–1274, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Friberg, R. Jennings, M. Alsarraj et al., “Indoleamine 2,3-dioxygenase contributes to tumor cell evasion of T cell-mediated rejection,” International Journal of Cancer, vol. 101, no. 2, pp. 151–155, 2002. View at Publisher · View at Google Scholar · View at Scopus
  24. M. D. Sharma, B. Baban, P. Chandler et al., “Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2,3-dioxygenase,” Journal of Clinical Investigation, vol. 117, no. 9, pp. 2570–2582, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. A. J. Muller and G. C. Prendergast, “Indoleamine 2,3-dioxygenase in immune suppression and cancer,” Current Cancer Drug Targets, vol. 7, no. 1, pp. 31–40, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. A. J. Muller, M. D. Sharma, P. R. Chandler et al., “Chronic inflammation that facilitates tumor progression creates local immune suppression by inducing indoleamine 2,3 dioxygenase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 44, pp. 17073–17078, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Godin-Ethier, L. A. Hanafi, C. A. Piccirillo, and R. Lapointe, “Indoleamine 2,3-dioxygenase expression in human cancers: clinical and immunologic perspectives,” Clinical Cancer Research, vol. 17, no. 22, pp. 6985–6991, 2011.
  28. D. H. Munn, A. L. Mellor, M. Rossi, and J. W. Young, “Dendritic cells have the option to express IDO-mediated suppression or not [4],” Blood, vol. 105, no. 6, p. 2618, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. N. Yoshida, K. Ino, Y. Ishida et al., “Overexpression of indoleamine 2,3-dioxygenase in human endometrial carcinoma cells induces rapidtumor growth in a mouse xenograft model,” Clinical Cancer Research, vol. 14, no. 22, pp. 7251–7259, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. O. Takikawa, T. Kuroiwa, F. Yamazaki, and R. Kido, “Mechanism of interferon-γ action. Characterization of indoleamine 2,3-dioxygenase in cultured human cells induced by interferon -γ and evaluation of the enzyme-mediated tryptophan degradation in its anticellular activity,” Journal of Biological Chemistry, vol. 263, no. 4, pp. 2041–2048, 1988. View at Scopus
  31. V. Levina, Y. Su, B. Nolen et al., “Chemotherapeutic drugs and human tumor cells cytokine network,” International Journal of Cancer, vol. 123, no. 9, pp. 2031–2040, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. C. J. Aslakson and F. R. Miller, “Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor,” Cancer Research, vol. 52, no. 6, pp. 1399–1405, 1992. View at Scopus
  33. B. A. Pulaski and S. Ostrand-Rosenberg, “Unit 20.2 mouse 4T1 breast tumor model,” in Current Protocols in Immunology, chapter 20, John Wiley & Sons, New York, NY, USA, 2001. View at Publisher · View at Google Scholar
  34. R. T. Reilly, M. B. C. Gottlieb, A. M. Ercolini et al., “HER-2/neu is a tumor rejection target in tolerized HER-2/neu transgenic mice,” Cancer Research, vol. 60, no. 13, pp. 3569–3576, 2000. View at Scopus
  35. M. B. Kastan and D. S. Lim, “The many substrates and functions of ATM,” Nature Reviews Molecular Cell Biology, vol. 1, no. 3, pp. 179–186, 2000. View at Scopus
  36. C. Laronga, H. Y. Yang, C. Neal, and M. H. Lee, “Association of the cyclin-dependent kinases and 14-3-3 sigma negatively regulates cell cycle progression,” Journal of Biological Chemistry, vol. 275, no. 30, pp. 23106–23112, 2000. View at Publisher · View at Google Scholar · View at Scopus
  37. X. Zheng, J. Koropatnick, M. Li et al., “Reinstalling antitumor immunity by inhibiting tumor-derived immunosuppressive molecule IDO through RNA interference,” Journal of Immunology, vol. 177, no. 8, pp. 5639–5646, 2006. View at Scopus
  38. G. C. Prendergast, R. Metz, and A. J. Muller, “Towards a genetic definition of cancer-associated inflammation: role of the IDO pathway,” American Journal of Pathology, vol. 176, no. 5, pp. 2082–2087, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. A. J. Muller, J. B. Duhadaway, D. Jaller, P. Curtis, R. Metz, and G. C. Prendergast, “Immunotherapeutic suppression of indoleamine 2,3-dioxygenase and tumor growth with ethyl pyruvate,” Cancer Research, vol. 70, no. 5, pp. 1845–1853, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Hill, V. Pereira, C. Chauveau et al., “Heme oxygenase-1 inhibits rat and human breast cancer cell proliferation: mutual cross inhibition with indoleamine 2,3-dioxygenase,” FASEB Journal, vol. 19, no. 14, pp. 1957–1968, 2005. View at Publisher · View at Google Scholar · View at Scopus