Non-tumor cell IDO1 predominantly contributes to enzyme activity and response to CTLA-4/PD-L1 inhibition in mouse glioblastoma

Brain, Behavior, and Immunity

Volumn 62, Issue , 2017, Pages 24-29

  Zhai, Lijie ^a   Ladomersky, Erik ^a   Dostal, Carlos R ^b   Lauing, Kristen L ^a   Swoap, Kathleen ^a   Billingham, Leah K ^a   Gritsina, Galina ^a   Wu, Meijing ^a   McCusker, Robert H ^b   Binder, David C ^c   Wainwright, Derek A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Glioma; IDO1; IDO2; Immunosuppression; Kynurenine; TDO2; Tryptophan

Indexed keywords

CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3 DIOXYGENASE 1; KYNURENINE; PROGRAMMED DEATH 1 LIGAND 1; UNCLASSIFIED DRUG; IDO1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CATABOLISM; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; GLIOBLASTOMA; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MOUSE; NONHUMAN; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL RATE; TUMOR IMMUNITY; TUMOR INVASION; ANIMAL; BRAIN; BRAIN TUMOR; DISEASE MODEL; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY;

ANIMALS; BRAIN; BRAIN NEOPLASMS; DISEASE MODELS, ANIMAL; GLIOBLASTOMA; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; KYNURENINE; MICE; MICE, KNOCKOUT;

EID: 85012892143     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2017.01.022     Document Type: Article

References (25)

1. Binder, D.C., Davis, A.A., Wainwright, D.A., Immunotherapy for cancer in the central nervous system: current and future directions. Oncoimmunol., 5, 2015, e1082027.
2. Carlin, J.M., Borden, E.C., Sondel, P.M., Byrne, G.I., Biologic-response-modifier-induced indoleamine 2,3-dioxygenase activity in human peripheral blood mononuclear cell cultures. J Immunol. 139 (1987), 2414–2418.
3. Chow, L.M., Endersby, R., Zhu, X., Rankin, S., Qu, C., Zhang, J., et al. Cooperativity within and among Pten, p53, and Rb pathways induces high-grade astrocytoma in adult brain. Cancer Cell 19 (2011), 305–316.
4. Curtin, J.F., Liu, N., Candolfi, M., Xiong, W., Assi, H., Yagiz, K., et al. HMGB1 mediates endogenous TLR2 activation and brain tumor regression. PLoS Med., 6, 2009, e10.
5. Fallarino, F., Grohmann, U., Vacca, C., Bianchi, R., Orabona, C., Spreca, A., et al. T cell apoptosis by tryptophan catabolism. Cell Death Differ. 9 (2002), 1069–1077.
6. Grohmann, U., Orabona, C., Fallarino, F., Vacca, C., Calcinaro, F., Falorni, A., et al. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat. Immunol. 3 (2002), 1097–1101.
7. Holmgaard, R.B., Zamarin, D., Munn, D.H., Wolchok, J.D., Allison, J.P., Indoleamine 2,3-dioxygenase is a critical resistance mechanism in antitumor T cell immunotherapy targeting CTLA-4. J. Exp. Med. 210 (2013), 1389–1402.
8. Hou, D.Y., Muller, A.J., Sharma, M.D., DuHadaway, J., Banerjee, T., Johnson, M., et al. Inhibition of indoleamine 2,3-dioxygenase in dendritic cells by stereoisomers of 1-methyl-tryptophan correlates with antitumor responses. Cancer Res. 67 (2007), 792–801.
9. Ladomersky, E., Genet, M., Zhai, L., Gritsina, G., Lauing, K.L., Fangusaro, J., et al. Improving Vaccine Efficacy Against Malignant Glioma. Oncoimmunol., 5, 2016, e1196311.
10. Larkin, J., Chiarion-Sileni, V., Gonzalez, R., Grob, J.J., Cowey, C.L., Lao, C.D., et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N. Engl. J. Med. 373 (2015), 23–34.
11. Lob, S., Konigsrainer, A., Zieker, D., Brucher, B.L., Rammensee, H.G., Opelz, G., et al. IDO1 and IDO2 are expressed in human tumors: levo- but not dextro-1-methyl tryptophan inhibits tryptophan catabolism. Cancer Immunol. Immunother. 58 (2009), 153–157.
12. Mezrich, J.D., Fechner, J.H., Zhang, X., Johnson, B.P., Burlingham, W.J., Bradfield, C.A., An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells. J Immunol. 185 (2010), 3190–3198.
13. Munn, D.H., Zhou, M., Attwood, J.T., Bondarev, I., Conway, S.J., Marshall, B., et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science (New York, NY) 281 (1998), 1191–1193.
14. Munn, D.H., Shafizadeh, E., Attwood, J.T., Bondarev, I., Pashine, A., Mellor, A.L., Inhibition of T cell proliferation by macrophage tryptophan catabolism. J. Exp. Med. 189 (1999), 1363–1372.
15. Munn, D.H., Blocking IDO activity to enhance anti-tumor immunity. Front. Biosci. (Elite ed.). 4 (2012), 734–745.
16. Pallotta, M.T., Orabona, C., Volpi, C., Vacca, C., Belladonna, M.L., Bianchi, R., et al. Indoleamine 2,3-dioxygenase is a signaling protein in long-term tolerance by dendritic cells. Nat. Immunol. 12 (2011), 870–878.
17. Reardon, D.A., Gilbert, M.R., Wick, W., Liau, L., Immunotherapy for neuro-oncology: the critical rationale for combinatorial therapy. Neuro Oncol. 17:Suppl 7 (2015), vii32–vii40.
18. Röhrig, U.F., Majjigapu, S.R., Vogel, P., Zoete, V., Michielin, O., Challenges in the Discovery of Indoleamine 2,3-Dioxygenase 1 (IDO1) Inhibitors. J. Med. Chem. 58 (2015), 9421–9437.
19. Stupp, R., Mason, W.P., van den Bent, M.J., Weller, M., Fisher, B., Taphoorn, M.J., et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 352 (2005), 987–996.
20. Uyttenhove, C., Pilotte, L., Theate, I., Stroobant, V., Colau, D., Parmentier, N., et al. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat. Med. 9 (2003), 1269–1274.
21. Wainwright, D.A., Balyasnikova, I.V., Chang, A.L., Ahmed, A.U., Moon, K.-S., Auffinger, B., et al. IDO Expression in Brain Tumors Increases the Recruitment of Regulatory T Cells and Negatively Impacts Survival. Clin. Cancer Res. 18 (2012), 6110–6121.
22. Wainwright, D.A., Chang, A.L., Dey, M., Balyasnikova, I.V., Kim, C., Tobias, A.L., et al. Durable therapeutic efficacy utilizing combinatorial blockade against IDO, CTLA-4 and PD-L1 in mice with brain tumors. Clin. Cancer Res. 20 (2014), 5290–5301.
23. Wolchok, J.D., Kluger, H., Callahan, M.K., Postow, M.A., Rizvi, N.A., Lesokhin, A.M., et al. Nivolumab plus ipilimumab in advanced melanoma. N. Engl. J. Med. 369 (2013), 122–133.
24. Zhai, L., Dey, M., Lauing, K.L., Gritsina, G., Kaur, R., Lukas, R.V., et al. The kynurenine to tryptophan ratio as a prognostic tool for glioblastoma patients enrolling in immunotherapy. J. Clin. Neurosci. 22 (2015), 1964–1968.
25. Zhai, L., Spranger, S., Binder, D.C., Gritsina, G., Lauing, K.L., Giles, F.J., et al. Molecular pathways: targeting IDO1 and other tryptophan dioxygenases for cancer immunotherapy. Clin. Cancer Res. 21 (2015), 5427–5433.