Indoleamine-2,3-dioxygenase in an immunotherapy model for Ewing sarcoma

Anticancer Research

Volumn 34, Issue 11, 2014, Pages 6431-6441

  Max, Daniela ^a   Kühnöl, Caspar D ^a   Burdach, Stefan ^a,b   Niu, Liguo ^c   Staege, Martin S ^a   Föll, Jürgen L ^a,d  

^a MARTIN LUTHER UNIVERSITÄT HALLE WITTENBERG   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY HOSPITAL REGENSBURG   (Germany)

Author keywords

CD137; Ewing sarcoma; Immune escape; Indoleamine 2,3 dioxygenase; Interleukin 2

Indexed keywords

CD137 ANTIGEN; CD137 LIGAND; GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; MESSENGER RNA; OX40 LIGAND;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER IMMUNOTHERAPY; CYTOKINE PRODUCTION; DOWN REGULATION; EWING SARCOMA; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE; ANIMAL; BONE NEOPLASMS; DISEASE MODEL; DRUG SCREENING; ENZYMOLOGY; FLOW CYTOMETRY; GENETICS; HUMAN; IMMUNOLOGY; IMMUNOTHERAPY; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SARCOMA, EWING; SCID MOUSE; TRANSGENIC MOUSE; TUMOR CELL CULTURE;

ANIMALS; ANTIGENS, CD137; BONE NEOPLASMS; CYTOKINES; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; HUMANS; IMMUNOTHERAPY; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTERFERON-GAMMA; INTERLEUKIN-2; LYMPHOCYTES; MICE; MICE, INBRED NOD; MICE, SCID; MICE, TRANSGENIC; OX40 LIGAND; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SARCOMA, EWING; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84916214562     PISSN: 02507005     EISSN: 17917530     Source Type: Journal    
DOI: None     Document Type: Article

References (73)

1. Burdach S, van Kaick B, Laws HJ, Ahrens S, Haase R, Körholz D, Pape H, Dunst J, Kahn T, Willers R, Engel B, Dirksen U, Kramm C, Nürnberger W, Heyll A, Ladenstein R, Gadner H, Jürgens H and Göbel U: Allogeneic and autologous stem-cell transplantation in advanced Ewing tumors. An update after longterm follow-up from two centers of the European Intergroup study EICESS. Stem-Cell Transplant Programs at Düsseldorf University Medical Center, Germany and St. Anna Kinderspital, Vienna, Austria. Ann Oncol 11: 1451-1462, 2000.
2. Staege MS and Max D: Genetics and epigenetics of the TETETS translocation network. Genetics and Epigenetics 2 : 1-15, 2009.
3. Staege MS, Hutter C, Neumann I, Foja S, Hattenhorst UE, Hansen G, Afar D and Burdach SE: DNA microarrays reveal relationship of Ewing family tumors to both endothelial and fetal neural crest-derived cells and define novel targets. Cancer Res 64 : 8213-8221, 2004.
4. Foell JL, Hesse M, Volkmer I, Schmiedel BJ, Neumann I and Staege MS: Membrane-associated phospholipase A1 beta (LIPI) is an Ewing tumour-associated cancer/testis antigen. Pediatr Blood Cancer 51: 228-234, 2008.
5. Max D, Hesse M, Volkmer I and Staege MS: High expression of the evolutionarily conserved alpha/beta hydrolase domain containing 6 (ABHD6) in Ewing tumors. Cancer Sci 100: 2383-2389, 2009.
6. Mahlendorf DE and Staege MS: Characterization of Ewing sarcoma associated cancer/testis antigens. Cancer Biol Ther 14: 254-261, 2013.
7. Vormoor J, Baersch G, Decker S, Hotfilder M, Schäfer KL, Pelken L, Rübe C, Van Valen F, Jürgens H and Dockhorn-Dworniczak B: Establishment of an in vivo model for pediatric Ewing tumors by transplantation into NOD/scid mice. Pediatr Res 49: 332-341, 2001.
8. Staege MS, Hansen G, Baersch G and Burdach S: Functional and molecular characterization of interleukin-2 transgenic Ewing tumor cells for in vivo immunotherapy. Pediatr Blood Cancer 43: 23-34, 2004.
9. Pollok KE, Kim YJ, Zhou Z, Hurtado J, Kim KK, Pickard RT and Kwon BS: Inducible T-cell antigen 4-1BB. Analysis of expression and function. J Immunol 150 : 771-781, 1993.
10. DeBenedette MA, Chu NR, Pollok KE, Hurtado J, Wade WF, Kwon BS and Watts TH: Role of 4-1BB ligand in co-stimulation of T-lymphocyte growth and its up-regulation on M12 B lymphomas by cAMP. J Exp Med 181: 985-992, 1995.
11. Hurtado JC, Kim YJ and Kwon BS: Signals through 4-1BB are co-stimulatory to previously activated splenic T-cells and inhibit activation-induced cell death. J Immunol 158: 2600-2609, 1997.
12. Ju SA, Lee SC, Kwon TH, Heo SK, Park SM, Paek HN, Suh JH, Cho HR, Kwon B, Kwon BS and Kim BS: Immunity to melanoma mediated by 4-1BB is associated with enhanced activity of tumour-infiltrating lymphocytes. Immunol Cell Biol 83: 344-351, 2005.
13. Mittler RS, Bailey TS, Klussman K, Trailsmith MD and Hoffmann MK: Anti-4-1BB monoclonal antibodies abrogate T-cell-dependent humoral immune responses in vivo through the induction of helper T-cell anergy. J Exp Med 190: 1535-1540, 1999.
14. Foell J, Strahotin S, O'Neil SP, McCausland MM, Suwyn C, Haber M, Chander PN, Bapat AS, Yan XJ, Chiorazzi N, Hoffmann MK and Mittler RS: CD137 co-stimulatory T-cell receptor engagement reverses acute disease in lupus-prone NZB x NZW F1 mice. J Clin Invest 111: 1505-1518, 2003.
15. Seo SK, Choi JH, Kim YH, Kang WJ, Park HY, Suh JH, Choi BK, Vinay DS and Kwon BS: 4-1BB-mediated immunotherapy of rheumatoid arthritis. Nat Med 10: 1088-1094, 2004.
16. Foell JL, Diez-Mendiondo BI, Diez OH, Holzer U, Ruck P, Bapat AS, Hoffmann MK, Mittler RS and Dannecker GE: Engagement of the CD137 (4-1BB) co-stimulatory molecule inhibits and reverses the autoimmune process in collagen-induced arthritis and establishes lasting disease resistance. Immunology 113: 89-98, 2004.
17. Melero I, Shuford WW, Newby SA, Aruffo A, Ledbetter JA, Hellström KE, Mittler RS and Chen L: Monoclonal antibodies against the 4-1BB T-cell activation molecule eradicate established tumors. Nat Med 3 : 682-685, 1997.
18. Wilcox RA, Flies DB, Zhu G, Johnson AJ, Tamada K, Chapoval AI, Strome SE, Pease LR and Chen L: Provision of antigen and CD137 signaling breaks immunological ignorance, promoting regression of poorly immunogenic tumors. J Clin Invest 109: 651-659, 2002.
19. Uyttenhove C, Pilotte L, Théate I, Stroobant V, Colau D, Parmentier N, Boon T and Van den Eynde BJ: Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine-2,3-dioxygenase. Nat Med 9: 1269-1274, 2003.
20. Munn DH, Sharma MD, Lee JR, Jhaver KG, Johnson TS, Keskin DB, Marshall B, Chandler P, Antonia SJ, Burgess R, Slingluff CL Jr and Mellor AL: Potential regulatory function of human dendritic cells expressing indoleamine-2,3-dioxygenase. Science 297: 1867-1870, 2002.
21. Biedler JL, Helson L and Spengler BA: Morphology and growth, tumorigenicity, and cytogenetics of human neuroblastoma cells in continuous culture. Cancer Res 33: 2643-2652, 1973.
22. Bloom ET: Further definition by cytotoxicity tests of cell surface antigens of human sarcomas in culture. Cancer Res 32: 960-967, 1972.
23. Whang-Peng J, Triche TJ, Knutsen T, Miser J, Kao-Shan S, Tsai S and Israel MA: Cytogenetic characterization of selected small round cell tumors of childhood. Cancer Genet Cytogenet 21: 185-208, 1986.
24. Tumilowicz JJ, Nichols WW, Cholon JJ, and Greene AE: Definition of a continuous human cell line derived from neuroblastoma. Cancer Res 30: 2110-2118, 1970.
25. Wolf J, Kapp U, Bohlen H, Kornacker M, Schoch C, Stahl B, Mücke S, von Kalle C, Fonatsch C, Schaefer HE, Hansmann ML and Diehl V: Peripheral blood mononuclear cells of a patient with advanced Hodgkin's lymphoma give rise to permanently growing Hodgkin-Reed Sternberg cells. Blood 87: 3418-3428, 1996.
26. Diehl V, Kirchner HH, Schaadt M, Fonatsch C, Stein H, Gerdes J and Boie C: Hodgkin's disease: establishment and characterization of four in vitro cell lines. J Cancer Res Clin Oncol 101: 111-124, 1981.
27. Drexler HG, Gaedicke G, Lok MS, Diehl V and Minowada J: Hodgkin's disease derived cell lines HDLM-2 and L-428: comparison of morphology, immunological and isoenzyme profiles. Leuk Res 10: 487-500, 1986.
28. Kamesaki H, Fukuhara S, Tatsumi E, Uchino H, Yamabe H, Miwa H, Shirakawa S, Hatanaka M and Honjo T: Cytochemical, immunologic, chromosomal, and molecular genetic analysis of a novel cell line derived from Hodgkin's disease. Blood 68: 285-292, 1986.
29. Tsuchiya S, Yamabe M, Yamaguchi Y, Kobayashi Y, Konno T and Tada K: Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int J Cancer 26: 171-176, 1980.
30. Lozzio CB and Lozzio BB: Cytotoxicity of a factor isolated from human spleen. J Natl Cancer Inst 50: 535-538, 1973.
31. Schneider U, Schwenk HU and Bornkamm G: Characterization of EBV-genome negative "null" and "T" cell lines derived from children with acute lymphoblastic leukemia and leukemic transformed non-Hodgkin lymphoma. Int J Cancer 19: 621-626, 1977.
32. Rasheed S, Nelson-Rees WA, Toth EM, Arnstein P and Gardner MB: Characterization of a newly derived human sarcoma cell line (HT-1080). Cancer 33 : 1027-1033, 1974.
33. Schere, WF, Syverton JT and Gey GO: Studies on the propagation in vitro of poliomyelitis viruses. IV. Viral multiplication in a stable strain of human malignant epithelial cells (strain HeLa) derived from an epidermoid carcinoma of the cervix. J Exp Med 97 : 695-710, 1953.
34. Giard DJ, Aaronson SA, Todaro GJ, Arnstein P, Kersey JH, Dosik H and Parks WP: In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. J Natl Cancer Inst 51: 1417-1423, 1973.
35. Sano K, Nakamura H, Mabuchi S, Tanaka T, Nakagawara A and Takai Y: Expression of the smg p25A (a ras p21-like GTPbinding protein) gene in human neuroblastoma cell lines and tumor tissues. Cancer Res 50: 7242-7245, 1990.
36. Staege MS, Gorelov V, Bulankin A, Fischer U, Dumon K, Hohndorf L, Hattenhorst U, Kramm C and Burdach S: Stable transgenic expression of IL2 and HSV1-tk by single and fusion tumor cell lines bearing EWS/FLI1 chimeric genes. Pediatr Hematol Oncol 20 : 119-140, 2003.
37. Collins SJ, Gallo RC and Gallagher RE: Continuous growth and differentiation of human myeloid leukaemic cells in suspension culture. Nature 270: 347-349. 1977.
38. Fabien N, Fusco A, Santoro M, Barbier Y, Dubois PM and Paulin C: Description of a human papillary thyroid carcinoma cell line. Morphologic study and expression of tumoral markers. Cancer 73: 2206-2212, 1994.
39. Goretzki PE, Frilling A, Simon D, Rastegar M and Ohmann C: Growth regulation of human thyrocytes by thyrotropin, cyclic adenosine monophosphate, epidermal growth factor and insulinlike growth factor. In : Frontiers of Hormone Research. Goretzki PE and Röher HD (eds.). Basel: Karger, pp. 56-80, 1989.
40. Ito T, Seyama T, Hayashi Y, Hayashi T, Dohi K, Mizuno T, Iwamoto K, Tsuyama N, Nakamura N and Akiyama M: Establishment of two human thyroid carcinoma cell lines (8305C, 8505C) bearing p53 gene mutations. Int J Oncol 4: 583-586, 1994.
41. Heldin NE, Cvejí D, Smeds S and Westermark B: Coexpression of functionally active receptors for thyrotropin and platelet-derived growth factor in human thyroid carcinoma cells. Endocrinology 129: 2187-2193, 1991.
42. Zucman J, Melot T, Desmaze C, Melot T, Desmaze C, Ghysdael J, Plougastel B, Peter M, Zucker JM, Triche TJ, Sheer D and Turc-Carel C: Combinatorial generation of variable fusion proteins in the Ewing family of tumours. EMBO J 12: 4481-4487, 1993.
43. Sorensen PH, Lessnick SL, Lopez-Terrada D, Liu XF, Triche TJ and Denny CT: A second Ewing's sarcoma translocation, t(21;22), fuses the EWS gene to another ETS-family transcription factor, ERG. Nat Genet 6: 146-151, 1994.
44. van Elsas A, Aarnoudse C, van der Minne CE, van der Spek CW, Brouwenstijn N, Osanto S and Schrier PI: Transfection of IL-2 augments CTL response to human melanoma cells in vitro: immunological characterization of a melanoma vaccine. J Immunother 20 : 343-353, 1997.
45. Miller G and Lipman M: Release of infectious Epstein-Barr virus by transformed marmoset leukocytes. Proc Natl Acad Sci USA 70: 190-194, 1973.
46. Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408, 2001.
47. Meisel R, Zibert A, Laryea M, Göbel U, Däubener W and Dilloo D: Human bone stromal cells inhibit allogenic responses by indoleamine-2,3-dioxygenase-mediated tryptophan degradation. Blood 103 : 4619-4621, 2004.
48. Zhang H, Merchant MS, Chua KS, Khanna C, Helman LJ, Telford B, Ward Y, Summers J, Toretsky J, Thomas EK, June CH and Mackall CL: Tumor expression of 4-1BB ligand sustains tumor lytic T-cells. Cancer Biol Ther 2: 579-586, 2003.
49. + T-cell proliferation and lead to the amplification in vivo of cytotoxic T-cell responses. J Exp Med 186 : 47-55, 1997.
50. Wilcox RA, Tamada K, Strome SE and Chen L: Signaling through NK cell-associated CD137 promotes both helper function for CD8+ cytolytic T-cells and responsiveness to IL2 but not cytolytic activity. J Immunol 169: 4230-4236, 2002.
51. Langstein J, Michel J, Fritsche J, Kreutz M, Andreesen R and Schwarz H: CD137 (ILA/4-1BB), a member of the TNF receptor family, induces monocyte activation via bidirectional signaling. J Immunol 160: 2488-2494, 1998.
52. Kienzle G and von Kempis J: CD137 (ILA/4-1BB), expressed by primary human monocytes, induces monocyte activation and apoptosis of B lymphocytes. Int Immunol 12: 73-82, 2000.
53. Babock TA and Carlin JM: Transcriptional activation of indolamine dioxygenase by interleukin 1 and tumor necrosis factor alpha in interferon-treated epithelial cells. Cytokine 12: 588-594, 2000.
54. Robinson CM, Shirey KA and Carlin JM: Synergistic transcriptional activation of indoleamine dioxygenase by IFN-gamma and tumor necrosis factor-alpha. J Interferon Cytokine Res 23: 413-421, 2003.
55. Li Q, Carr A, Ito F, Teitz-Tennenbaum S and Chang AE: Polarization effects of 4-1BB during CD28 costimulation in generating tumor-reactive T-cells for cancer immunotherapy. Cancer Res 63: 2546-2552, 2003.
56. Jiang D, Chen Y and Schwarz H: CD137 induces proliferation of murine hematopoietic progenitor cells and differentiation to macrophages. J Immunol 181: 3923-3932, 2008.
57. Zhang B, Maris CH, Foell J, Whitmire J, Niu L, Song J, Kwon BS, Vella AT, Ahmed R, Jacob J and Mittler RS: Immune suppression or enhancement by CD137 T cell co-stimulation during acute viral infection is time dependent. J Clin Invest 117: 3029-3041, 2007.
58. Shin HH, Lee JE and Choi HS: Absence of 4-1BB increases cell influx into the peritoneal cavity in response to LPS stimulation by decreasing macrophage IL10 levels. FEBS Lett 581: 4355-4360, 2007.
59. Ito F, Li Q, Shreiner AB, Okuyama R, Jure-Kunkel MN, Teitz-Tennenbaum S and Chang AE: Anti-CD137 monoclonal antibody administration augments the antitumor efficacy of dendritic cell-based vaccines. Cancer Res 64: 8411-8419, 2004.
60. Carlin JM, Borden EC, Sondel PM and Byrne GI: Biologic-response-modifier-induced indoleamine-2,3-dioxygenase activity in human peripheral blood mononuclear cell cultures. J Immunol 139: 2414-2418, 1987.
61. Werner-Felmayer G, Werner ER, Fuchs D, Hausen A, Reibnegger G and Wachter H: Characteristics of interferon induced tryptophan metabolism in human cells in vitro. Biochem Biophys Acta 1012: 142-147, 1998.
62. Takikawa O, Kuroiwa T, Yamazaki F and Kido R: Mechanism of interferon-gamma action. Characterization of indoleamine-2,3-dioxygenase in cultured human cells induced by interferongamma and evaluation of the enzyme-mediated tryptophan degradation in its anticellular activity. J Biol Chem 263: 2041-2048, 1988.
63. Chen PW, Mellon JK, Mayhew E, Wang S, He YG, Hogan N and Niederkorn JY: Uveal melanoma expression of indoleamine-2,3-deoxygenase: establishment of an immune privileged environment by tryptophan depletion. Exp Eye Res 85: 617-625, 2007.
64. Ozaki Y, Edelstein MP and Duch DS: Induction of indoleamine 2,3-dioxygenase: a mechanism of the antitumor activity of interferon gamma. Proc Natl Acad Sci USA 85: 1242-1246, 1988.
65. Edelstein M P, Ozaki Y and Duch DS: Synergistic effects of phorbol ester and INF-gamma on the induction of indoleamine-2,3-dioxygenase in THP-1 monocytic leukemia cells. J Immunol 143: 2969-2673, 1989.
66. Melichar B, Hu W, Patenia R, Melicharová K, Gallardo ST and Freedman: rIFN-gamma-mediated growth suppression of platinum-sensitive and -resistant ovarian tumor cell lines not dependent upon arginase inhibition. J Transl Med 19: 5, 2003.
67. Pan K, Wang H, Chen MS, Zhang HK, Weng DS, Zhou J, Huang W, Li JJ, Song HF and Xia JC: Expression and prognosis role of indoleamine-2,3-dioxygenase in hepatocellular carcinoma. J Cancer Res Clin Oncol 134: 1247-1253, 2008.
68. Brandacher G, Perathoner A, Ladurner R, Schneeberger S, Obrist P, Winkler C, Werner ER, Werner-Felmayer G, Weiss HG, Göbel G, Margreiter R, Königsrainer A, Fuchs D and Amberger A:. Prognostic value of indoleamine-2,3-dioxygenase expression in colorectal cancer: effect on tumor-infiltrating T-cells. Clin. Cancer Res 12: 1144-1151, 2006.
69. Riesenberg R, Weiler C, Spring O, Eder M, Buchner A, Popp T, Castro M, Kammerer R, Takikawa O, Hatz RA, Stief CG, Hofstetter A and Zimmermann W: Expression of indoleamine-2,3-dioxygenase in tumor endothelial cells correlates with longterm survival of patients with renal cell carcinoma. Clin Cancer Res 13: 6993-7002, 2007.
70. Phan-Bich L, Buard A, Petit JF, Zeng L, Tenu JP, Chretien P, Monnet I, Boutin C, Bignon J, Lemaire G and Jaurand MC: Differential responsiveness of human and rat mesothelioma cell lines to recombinant interferon-gamma. Am J Respir Cell Mol Biol 16: 178-186, 1997.
71. Curti A, Pandolfi S, Valzasina B, Aluigi M, Isidori A, Ferri E, Salvestrini V, Bonanno G, Rutella S, Durelli I, Horenstein AL, Fiore F, Massaia M, Colombo MP, Baccarani M and Lemoli RM: Modulation of tryptophan catabolism by human leukemic cells results in the conversion of CD25- into CD25+ Tregulatory cells. Blood 109: 2871-2877, 2007.
72. Hoshi M, Ito H, Fujigaki H, Takemura M, Takahashi T, Tomita E, Ohyama M, Tanaka R, Saito K and Seishima M: Indoleamine-2,3-dioxygenase is highly expressed in human adult T-cell leukemia/lymphoma and chemotherapy changes tryptophan catabolism in serum and reduced activity. Leuk Res 33: 39-45, 2009.
73. Chamuleau ME, van de Loosdrecht AA, Hess CJ, Janssen JJ, Zevenbergen A, Delwel R, Valk PJ, Löwenberg B and Ossenkoppele GJ: High INDO (indoleamine-2,3-dioxygenase) mRNA level in blasts of acute myeloid leukemic patients predicts poor clinical outcome. Haematologica 93: 1894-1898, 2008.