Inhibition of indoleamine 2,3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy

Nature Medicine

Volumn 11, Issue 3, 2005, Pages 312-319

  Muller, Alexander J ^a   DuHadaway, James B ^a   Donover, P Scott ^a   Sutanto Ward, Erika ^a   Prendergast, George C ^a,b  

^a LANKENAU INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; CYCLOPHOSPHAMIDE; CYTOTOXIC AGENT; DOXORUBICIN; ENZYME INHIBITOR; FLUOROURACIL; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 2; LUCIFERASE; METHOTREXATE; METHYLTHIOHYDANTOINTRYPTOPHAN; N METHYLTRYPTOPHAN; NICOTINAMIDE ADENINE DINUCLEOTIDE; PACLITAXEL; RAPAMYCIN; SMALL INTERFERING RNA; STAT1 PROTEIN; TETRATHIOMOLYBDIC ACID; THIOHYDANTOIN DERIVATIVE; TRYPTOPHAN; TRYPTOPHAN DERIVATIVE; UNCLASSIFIED DRUG; VINBLASTINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; BIN1 GENE; BREAST CANCER; CANCER CHEMOTHERAPY; CELL PROLIFERATION; CELL STRAIN COS1; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; EMBRYO; ENZYME INHIBITION; HELA CELL; HUMAN; HUMAN CELL; IMMUNE ESCAPE; IMMUNOMODULATION; KNOCKOUT MOUSE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; T LYMPHOCYTE; TUMOR GROWTH; TUMOR IMMUNITY; TUMOR REGRESSION; TUMOR SUPPRESSOR GENE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; DNA-BINDING PROTEINS; DRUG SYNERGISM; ENZYME INHIBITORS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INDOLES; INTERFERON TYPE II; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NF-KAPPA B; PACLITAXEL; RATS; STAT1 TRANSCRIPTION FACTOR; THIOHYDANTOINS; TRANS-ACTIVATORS; TRYPTOPHAN OXYGENASE; TUMOR ESCAPE; TUMOR SUPPRESSOR PROTEINS;

EID: 16244408626     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/nm1196     Document Type: Article

References (50)

1. Dranoff, G. Cytokines in cancer pathogenesis and cancer therapy. Nat. Rev. Cancer 4, 11-22 (2004).
2. Marincola, F.M., Jaffee, E.M., Hicklin, D.J. & Ferrone, S. Escape of human solid tumors from T-cell recognition: molecular mechanisms and functional significance. Adv. Immunol. 74, 181-273 (2000).
3. Sakamuro, D., Elliott, K., Wechsler-Reya, R. & Prendergast, G.C. BIN1 is a novel MYC-interacting protein with features of a tumor suppressor. Nat. Genet. 14, 69-77 (1996).
4. Elliott, K. et al. Bin1 functionally interacts with Myc in cells and inhibits cell proliferation by multiple mechanisms. Oncogene 18, 3564-3573 (1999).
5. Ge, K. et al. Mechanism for elimination of a tumor suppressor: aberrant splicing of a brain-specific exon causes loss of function of Bin1 in melanoma. Proc. Natl. Acad. Sci. USA 96, 9689-9694 (1999).
6. Ge, K. et al. Losses of the tumor suppressor Bin1 in breast carcinoma are frequent and reflect deficits in a programmed cell death capacity. Int. J. Cancer 85, 376-383 (2000).
7. Ge, K. et al. Loss of heterozygosity and tumor suppressor activity of Bin1 in prostate carcinoma. Int. J. Cancer 86, 155-161 (2000).
8. Tajiri, T. et al. Expression of a MYCN-interacting isoform of the tumor suppressor BIN1 is reduced in neuroblastomas with unfavorable biological features. Clin. Cancer Res. 9, 3345-3355 (2003).
9. Muller, A.J., DuHadaway, J.B., Donover, P.S., Sutanto-Ward, E. & Prendergast, G.C. Targeted deletion of the suppressor gene Bin1/Amphiphysin2 enhances the malignant character of transformed cells. Cancer Biol. Ther. 3, published online 14 December 2004.
10. Wigge, P. & McMahon, H.T. The amphiphysin family of proteins and their role in endocytosis at the synapse. Trends Neurosci. 21, 339-344 (1998).
11. Zelhof, A.C. et al. Drosophila Amphiphysin is implicated in protein localization and membrane morphogenesis but not in synaptic vesicle endocytosis. Development 128, 5005-5015 (2001).
12. Muller, A.J. et al. Targeted disruption of the murine Bin1/Amphiphysin II gene does not disable endocytosis but results in embryonic cardiomyopathy with aberrant myofibril formation. Mol. Cell. Biol. 23, 4295-4306 (2003).
13. Routhier, E.L., Donover, P.S. & Prendergast, G.C. hob1+, the homolog of Bin1 in fission yeast, is dispensable for endocytosis but required for the response to starvation or genotoxic stress. Oncogene 22, 637-648 (2003).
14. Leprince, C. et al. Sorting nexin 4 and amphiphysin 2, a new partnership between endocytosis and intracellular trafficking. J. Cell Sci. 116, 1937-1948 (2003).
15. Peter, B.J. et al. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495-499 (2003).
16. Miaczynska, M. et al. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 116, 445-456 (2004).
17. Munn, D.H. et al. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J. Exp. Med. 189, 1363-1372 (1999).
18. Grohmann, U., Fallarino, F. & Puccetti, P. Tolerance, DCs and tryptophan: much ado about IDO. Trends Immunol. 24, 242-248 (2003).
19. Munn, D.H. et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281, 1191-1193 (1998).
20. Friberg, M. et al. Indoleamine 2,3-dioxygenase contributes to tumor cell evasion of T cell-mediated rejection. Int. J. Cancer 101, 151-155 (2002).
21. Uyttenhove, C. et al. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat. Med. 3, 1269-1274 (2003).
22. DuHadaway, J.B., Sakamuro, D., Ewert, D.L. & Prendergast, G.C. Bin1 mediates apoptosis by c-Myc in transformed primary cells. Cancer Res. 16, 3151-3156 (2001).
23. Debrick, J.E., Campbell, P.A. & Staerz, U.D. Macrophages as accessory cells for class I MHC-restricted immune responses. J. Immunol. 147, 2846-2851 (1991).
24. Bild, A.H., Turkson, J. & Jove, R. Cytoplasmic transport of Stat3 by receptor-mediated endocytosis. EMBO J. 21, 3255-3263 (2002).
25. Shimizu, F., Satoh, J., Tada, M. & Kumagai, K. Suppression of in vitro growth of virulent and avirulent herpes simplex viruses by cell-mediated immune mechanisms, antibody, and interferon. Infect. Immun. 22, 752-577 (1978).
26. Du, M.X., Sotero-Esteva, W.D. & Taylor, M.W. Analysis of transcription factors regulating induction of indoleamine 2,3-dioxygenase by IFN-gamma. J. Interferon Cytokine Res. 20, 133-142 (2000).
27. Mason, K. et al. Enhancement of tumor radioresponse by docetaxel: involvement of immune system. Int. J. Oncol. 18, 599-606 (2001).
28. Brandt, R., Wong, A.M. & Hynes, N.E. Mammary glands reconstituted with Neu/ErbB2 transformed HC11 cells provide a novel orthotopic tumor model for testing anti-cancer agents. Oncogene 20, 5459-5465 (2001).
29. Kohl, N.E. et al. Inhibition of farnesyltransferase induces regression of mammary and salivary carcinomas in ras transgenic mice. Nat. Med. 1, 792-797 (1005).
30. Littlejohn, T.K. et al. Expression and purification of recombinant human indoleamine 2,3-dioxygenase. Prot. Exp. Purif. 19, 22-29 (2000).
31. Hanahan, D. & Weinberg, R.A. The hallmarks of cancer. Cell 100, 57-70 (2000).
32. Huang, H. et al. Gene expression profiling of low-grade diffuse astrocytomas by cDNA arrays. Cancer Res. 60, 6868-6874 (2000).
33. DuHadaway, J.B. et al. Immunohistochemical analysis of Bin1/Amphiphysin II in human tissues: Diverse sites of nuclear expression and losses in prostate cancer. J. Cell. Biochem. 88, 635-642 (2003).
34. Nowak, A.K., Robinson, B.W. & Lake, R.A. Synergy between chemotherapy and immunotherapy in the treatment of established murine solid tumors. Cancer Res. 63, 4490-4496 (2003).
35. Machiels, J.P. et al. Cyclophosphamide, doxorubicin, and paclitaxel enhance the antitumor immune response of granulocyte/macrophage-colony stimulating factor-secreting whole-cell vaccines in HER-2/neu tolerized mice. Cancer Res. 61, 3689-3697 (2001).
36. Wechsler-Reya, R., Elliott, K., Herlyn, M. & Prendergast, G.C. The putative tumor suppressor BIN1 is a short-lived nuclear phosphoprotein whose localization is altered in malignant cells. Cancer Res. 57, 3258-3263 (1997).
37. Wechsler-Reya, R., Elliott, K. & Prendergast, G.C. A role for the putative tumor suppressor Bin1 in muscle cell differentiation. Mol. Cell. Biol. 18, 566-575 (1998).
38. Meloni, A.R., Smith, E.J. & Nevins, J.R. A mechanism for Rb/p130-mediated transcription repression involving recruitment of the CtBP corepressor. Proc. Natl. Acad. Sci. USA 96, 9574-9579 (1999).
39. Weigert, R. et al. CtBP/BARS induces fission of Golgi membranes by acylating lysophosphatidic acid. Nature 402, 429-433 (1999).
40. Vecchi, M. et al. Nucleocytoplasmic shuttling of endocytic proteins. J. Cell Biol. 153, 1511-1517 (2001).
41. DuHadaway, J.B. et al. Transformation selective apoptosis by farnesyltransferase inhibitors requires Bin1. Oncogene 22, 3578-3588 (2003).
42. Elliott, K., Ge, K., Du, W. & Prendergast, G.C. The c-Myc-interacting adapter protein Bin1 activates a caspase-independent cell death program. Oncogene 19, 4669-4684 (2000).
43. Bernards, R., Dessain, S.K. & Weinberg, R.A. N-myc amplification causes down-modulation of MHC class I antigen expression in neuroblastoma. Cell 47, 667-674 (1986).
44. Versteeg, R., Noordermeer, I.A., Kruse-Wolters, M., Ruiter, D.J. & Schrier, P.I. c-myc down-regulates class I HLA expression in human melanomas. EMBO J. 7, 1023-1029 (1988).
45. Boyland, E. & Willliams, D.C. The metabolism of tryptophan. 2. The metabolism of tryptophan in patients suffering from cancer of the bladder. Biochem. J. 64, 578-582 (1956).
46. Rose, D. Tryptophan metabolism in carcinoma of the breast. Lancet 1, 239-241 (1967).
47. Munn, D.H. et al. Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science 297, 1867-1870 (2002).
48. Gilmour, S.K., Birchler, M., Smith, M.K., Rayca, K. & Mostochuk, J. Effect of elevated levels of ornithine decarboxylase on cell cycle progression in skin. Cell Growth Differ. 10, 739-748 (1999).
49. Koprowski, H. et al. Colorectal carcinoma antigens detected by hybridoma antibodies. Som. Cell Genet. 5, 957-972 (1979).
50. Kruisbeek, A. In vivo depletion of CD4- and CD8-specific T cells. in Current Protocols in Immunology (eds. Coligan, J.E., Kruisbeek, A.M., Margulies, D.H., Shevach, E.M. & Strober, W.) p. 4.1.1-4.1.5 (John Wiley & Sons, Inc., New York, 1991).