PEG-rIL-10 treatment decreases FoxP3⁺ Tregs despite upregulation of intratumoral IDO

References

• de Waal Malefyt R, Abrams J, Bennett B, Figdor CG, de Vries JE. Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med 1991; 174:1209-20; PMID:1940799; http://dx.doi.org/10.1084/jem.174.5.1209
   PubMed Web of Science ®Google Scholar
• de Waal Malefyt R, Haanen J, Spits H, Roncarolo MG, te Velde A, Figdor C, Johnson K, Kastelein R, Yssel H, de Vries JE. Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J Exp Med 1991; 174:915-24; PMID:1655948; http://dx.doi.org/10.1084/jem.174.4.915
   PubMed Web of Science ®Google Scholar
• Akdis CA, Joss A, Akdis M, Faith A, Blaser K. A molecular basis for T cell suppression by IL-10: CD28-associated IL-10 receptor inhibits CD28 tyrosine phosphorylation and phosphatidylinositol 3-kinase binding. FASEB J: Off Pub Federat Am Soc Exp Biol 2000; 14:1666-8; PMID:10973911; http://dx.doi.org/10.1096/fj.99-0874fje
   PubMed Web of Science ®Google Scholar
• Joss A, Akdis M, Faith A, Blaser K, Akdis CA. IL-10 directly acts on T cells by specifically altering the CD28 co-stimulation pathway. Euro J Immunol 2000; 30:1683-90; PMID:10898505; http://dx.doi.org/10.1002/1521-4141(200006)30:6%3c1683::AID-IMMU1683%3e3.0.CO;2-A
   PubMed Web of Science ®Google Scholar
• Opp MR, Smith EM, Hughes TK, Jr. Interleukin-10 (cytokine synthesis inhibitory factor) acts in the central nervous system of rats to reduce sleep. J Neuroimmunol 1995; 60:165-8; PMID:7642744; http://dx.doi.org/10.1016/0165-5728(95)00066-B
   PubMed Web of Science ®Google Scholar
• Aste-Amezaga M, Ma X, Sartori A, Trinchieri G. Molecular mechanisms of the induction of IL-12 and its inhibition by IL-10. J Immunol 1998; 160:5936-44; PMID:9637507
   PubMed Web of Science ®Google Scholar
• Varma TK, Toliver-Kinsky TE, Lin CY, Koutrouvelis AP, Nichols JE, Sherwood ER. Cellular mechanisms that cause suppressed gamma interferon secretion in endotoxin-tolerant mice. Infect Immun 2001; 69:5249-63; PMID:11500393; http://dx.doi.org/10.1128/IAI.69.9.5249-5263.2001
   PubMed Web of Science ®Google Scholar
• Zheng LM, Ojcius DM, Garaud F, Roth C, Maxwell E, Li Z, Rong H, Chen J, Wang XY, Catino JJ et al. Interleukin-10 inhibits tumor metastasis through an NK cell-dependent mechanism. J Exp Med 1996; 184:579-84; PMID:8760811; http://dx.doi.org/10.1084/jem.184.2.579
   PubMed Web of Science ®Google Scholar
• Sun H, Gutierrez P, Jackson MJ, Kundu N, Fulton AM. Essential role of nitric oxide and interferon-gamma for tumor immunotherapy with interleukin-10. J Immunother 2000; 23:208-14; PMID:10746547; http://dx.doi.org/10.1097/00002371-200003000-00005
   PubMed Web of Science ®Google Scholar
• Sun H, Jackson MJ, Kundu N, Fulton AM. Interleukin-10 gene transfer activates interferon-gamma and the interferon-gamma-inducible genes Gbp-1/Mag-1 and Mig-1 in mammary tumors. Int J Cancer J Int du Cancer 1999; 80:624-9; PMID:9935167; http://dx.doi.org/10.1002/(SICI)1097-0215(19990209)80:4%3c624::AID-IJC23%3e3.0.CO;2-9
   PubMed Web of Science ®Google Scholar
• Groux H, Cottrez F, Rouleau M, Mauze S, Antonenko S, Hurst S, McNeil T, Bigler M, Roncarolo MG, Coffman RL. A transgenic model to analyze the immunoregulatory role of IL-10 secreted by antigen-presenting cells. J Immunol 1999; 162:1723-9; PMID:9973435
   PubMed Web of Science ®Google Scholar
• Fujii S, Shimizu K, Shimizu T, Lotze MT. Interleukin-10 promotes the maintenance of antitumor CD8(+) T-cell effector function in situ. Blood 2001; 98:2143-51; PMID:11568001; http://dx.doi.org/10.1182/blood.V98.7.2143
   PubMed Web of Science ®Google Scholar
• Berman RM, Suzuki T, Tahara H, Robbins PD, Narula SK, Lotze MT. Systemic administration of cellular IL-10 induces an effective, specific, and long-lived immune response against established tumors in mice. J Immunol 1996; 157:231-8; PMID:8683120
   PubMed Web of Science ®Google Scholar
• Suzuki T, Tahara H, Narula S, Moore KW, Robbins PD, Lotze MT. Viral interleukin 10 (IL-10), the human herpes virus 4 cellular IL-10 homologue, induces local anergy to allogeneic and syngeneic tumors. J Exp Med 1995; 182:477-86; PMID:7629507; http://dx.doi.org/10.1084/jem.182.2.477
   PubMed Web of Science ®Google Scholar
• Emmerich J, Mumm JB, Chan IH, LaFace D, Truong H, McClanahan T, Gorman DM, Oft M. IL-10 directly activates and expands tumor-resident CD8(+) T cells without de novo infiltration from secondary lymphoid organs. Cancer Res 2012; 72:3570-81; PMID:22581824; http://dx.doi.org/10.1158/0008-5472.CAN-12-0721
   PubMed Web of Science ®Google Scholar
• Mumm JB, Emmerich J, Zhang X, Chan I, Wu L, Mauze S, Blaisdell S, Basham B, Dai J, Grein J et al. IL-10 elicits IFNgamma-dependent tumor immune surveillance. Cancer Cell 2011; 20:781-96; PMID:22172723; http://dx.doi.org/10.1016/j.ccr.2011.11.003
   PubMed Web of Science ®Google Scholar
• Infante JR, Naing A, Papadopoulos KP, Autio KA, Ott PA, Wong DJL, Falchook GS, Patel MR, Pant S, Whiteside M et al. A first-in-human dose escalation study of PEGylated recombinant human IL-10 (AM0010) in advanced solid tumors. ASCO Meeting Abstracts 2015; 33:3017
   Google Scholar
• Mellor AL, Munn DH. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol 2004; 4:762-74; PMID:15459668; http://dx.doi.org/10.1038/nri1457
   PubMed Web of Science ®Google Scholar
• Munn DH, Mellor AL. IDO and tolerance to tumors. Trends Mol Med 2004; 10:15-8; PMID:14720581; http://dx.doi.org/10.1016/j.molmed.2003.11.003
   PubMed Web of Science ®Google Scholar
• Huang L, Li L, Klonowski KD, Tompkins SM, Tripp RA, Mellor AL. Induction and role of indoleamine 2,3 dioxygenase in mouse models of influenza a virus infection. PloS One 2013; 8:e66546; PMID:23785507; http://dx.doi.org/10.1371/journal.pone.0066546
   PubMed Web of Science ®Google Scholar
• Sakash JB, Byrne GI, Lichtman A, Libby P. Cytokines induce indoleamine 2,3-dioxygenase expression in human atheroma-associated cells: implications for persistent Chlamydophila pneumoniae infection. Infect Immun 2002; 70:3959-61; PMID:12065543; http://dx.doi.org/10.1128/IAI.70.7.3959-3961.2002
   PubMed Web of Science ®Google Scholar
• Fujigaki S, Saito K, Sekikawa K, Tone S, Takikawa O, Fujii H, Wada H, Noma A, Seishima M. Lipopolysaccharide induction of indoleamine 2,3-dioxygenase is mediated dominantly by an IFN-gamma-independent mechanism. Euro J Immunol 2001; 31:2313-8; PMID:11477543; http://dx.doi.org/10.1002/1521-4141(200108)31:8%3c2313::AID-IMMU2313%3e3.0.CO;2-S
   PubMed Web of Science ®Google Scholar
• Frumento G, Rotondo R, Tonetti M, Damonte G, Benatti U, Ferrara GB. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. J Exp Med 2002; 196:459-68; PMID:12186838; http://dx.doi.org/10.1084/jem.20020121
   PubMed Web of Science ®Google Scholar
• Curti A, Pandolfi S, Valzasina B, Aluigi M, Isidori A, Ferri E, Salvestrini V, Bonanno G, Rutella S, Durelli I et al. Modulation of tryptophan catabolism by human leukemic cells results in the conversion of CD25- into CD25+ T regulatory cells. Blood 2007; 109:2871-7; PMID:17164341; http://dx.doi.org/10.1182/blood-2006-07-036863
   PubMed Web of Science ®Google Scholar
• Wainwright DA, Dey M, Chang A, Lesniak MS. Targeting tregs in malignant brain cancer: overcoming IDO. Front Immunol 2013; 4:116; PMID:23720663; http://dx.doi.org/10.3389/fimmu.2013.00116
   PubMed Web of Science ®Google Scholar
• Baban B, Chandler PR, Sharma MD, Pihkala J, Koni PA, Munn DH, Mellor AL. IDO activates regulatory T cells and blocks their conversion into Th17-like T cells. J Immunol 2009; 183:2475-83; PMID:19635913; http://dx.doi.org/10.4049/jimmunol.0900986
   PubMed Web of Science ®Google Scholar
• Chan IH, Wu V, Bilardello M, Mar E, Oft M, Van Vlasselaer P, Mumm JB. The potentiation of IFN-gamma and induction of cytotoxic proteins by pegylated IL-10 in human CD8 T cells. J Interferon Cytokine Res 2015; PMID:26309093; http://dx.doi.org/10.1089/jir.2014.0221
   PubMed Web of Science ®Google Scholar
• Taylor MW, Feng GS. Relationship between interferon-gamma, indoleamine 2,3-dioxygenase, and tryptophan catabolism. FASEB J: Off Pub Federat Am Soc Exp Biol 1991; 5:2516-22; PMID:1907934
   PubMed Web of Science ®Google Scholar
• Jurgens B, Hainz U, Fuchs D, Felzmann T, Heitger A. Interferon-gamma-triggered indoleamine 2,3-dioxygenase competence in human monocyte-derived dendritic cells induces regulatory activity in allogeneic T cells. Blood 2009; 114:3235-43; PMID:19625705; http://dx.doi.org/10.1182/blood-2008-12-195073
   PubMed Web of Science ®Google Scholar
• Sarkar SA, Wong R, Hackl SI, Moua O, Gill RG, Wiseman A, Davidson HW, Hutton JC. Induction of indoleamine 2,3-dioxygenase by interferon-gamma in human islets. Diabetes 2007; 56:72-9; PMID:17192467; http://dx.doi.org/10.2337/db06-0617
   PubMed Web of Science ®Google Scholar
• Liu X, Shin N, Koblish HK, Yang G, Wang Q, Wang K, Leffet L, Hansbury MJ, Thomas B, Rupar M et al. Selective inhibition of IDO1 effectively regulates mediators of antitumor immunity. Blood 2010; 115:3520-30; PMID:20197554; http://dx.doi.org/10.1182/blood-2009-09-246124
   PubMed Web of Science ®Google Scholar
• Jana S, Jailwala P, Haribhai D, Waukau J, Glisic S, Grossman W, Mishra M, Wen R, Wang D, Williams CB et al. The role of NF-kappaB and Smad3 in TGF-beta-mediated Foxp3 expression. Euro J Immunol 2009; 39:2571-83; PMID:19701891; http://dx.doi.org/10.1002/eji.200939201
   PubMed Web of Science ®Google Scholar
• Fu S, Zhang N, Yopp AC, Chen D, Mao M, Chen D, Zhang H, Ding Y, Bromberg JS. TGF-beta induces Foxp3 + T-regulatory cells from CD4 + CD25 - precursors. Am J Transplant 2004; 4:1614-27; PMID:15367216; http://dx.doi.org/10.1111/j.1600-6143.2004.00566.x
   PubMed Web of Science ®Google Scholar
• Tran DQ, Ramsey H, Shevach EM. Induction of FOXP3 expression in naive human CD4+FOXP3 T cells by T-cell receptor stimulation is transforming growth factor-beta dependent but does not confer a regulatory phenotype. Blood 2007; 110:2983-90; PMID:17644734; http://dx.doi.org/10.1182/blood-2007-06-094656
   PubMed Web of Science ®Google Scholar
• Chen Q, Kim YC, Laurence A, Punkosdy GA, Shevach EM. IL-2 controls the stability of Foxp3 expression in TGF-beta-induced Foxp3+ T cells in vivo. J Immunol 2011; 186:6329-37; PMID:21525380; http://dx.doi.org/10.4049/jimmunol.1100061
   PubMed Web of Science ®Google Scholar
• Van Vlasselaer P, Borremans B, van Gorp U, Dasch JR, De Waal-Malefyt R. Interleukin 10 inhibits transforming growth factor-beta (TGF-beta) synthesis required for osteogenic commitment of mouse bone marrow cells. J Cell Biol 1994; 124:569-77; PMID:8106554; http://dx.doi.org/10.1083/jcb.124.4.569
   PubMed Web of Science ®Google Scholar
• Nakagome K, Dohi M, Okunishi K, Tanaka R, Miyazaki J, Yamamoto K. In vivo IL-10 gene delivery attenuates bleomycin induced pulmonary fibrosis by inhibiting the production and activation of TGF-beta in the lung. Thorax 2006; 61:886-94; PMID:16809410; http://dx.doi.org/10.1136/thx.2005.056317
   PubMed Web of Science ®Google Scholar
• Fedorak RN, Gangl A, Elson CO, Rutgeerts P, Schreiber S, Wild G, Hanauer SB, Kilian A, Cohard M, LeBeaut A et al. Recombinant human interleukin 10 in the treatment of patients with mild to moderately active Crohn's disease. The interleukin 10 inflammatory bowel disease cooperative study group. Gastroenterology 2000; 119:1473-82; PMID:11113068; http://dx.doi.org/10.1053/gast.2000.20229
   PubMed Web of Science ®Google Scholar
• Schreiber S, Fedorak RN, Nielsen OH, Wild G, Williams CN, Nikolaus S, Jacyna M, Lashner BA, Gangl A, Rutgeerts P et al. Safety and efficacy of recombinant human interleukin 10 in chronic active Crohn's disease. Crohn's disease IL-10 cooperative study group. Gastroenterology 2000; 119:1461-72; PMID:11113067; http://dx.doi.org/10.1053/gast.2000.20196
   PubMed Web of Science ®Google Scholar
• Asadullah K, Docke WD, Ebeling M, Friedrich M, Belbe G, Audring H, Volk HD, Sterry W. Interleukin 10 treatment of psoriasis: clinical results of a phase 2 trial. Arch Dermatol 1999; 135:187-92; PMID:10052405; http://dx.doi.org/10.1001/archderm.135.2.187
   PubMed Web of Science ®Google Scholar
• Tilg H, van Montfrans C, van den Ende A, Kaser A, van Deventer SJ, Schreiber S, Gregor M, Ludwiczek O, Rutgeerts P, Gasche C et al. Treatment of Crohn's disease with recombinant human interleukin 10 induces the proinflammatory cytokine interferon gamma. Gut 2002; 50:191-5; PMID:11788558; http://dx.doi.org/10.1136/gut.50.2.191
   PubMed Web of Science ®Google Scholar
• Lauw FN, Pajkrt D, Hack CE, Kurimoto M, van Deventer SJ, van der Poll T. Proinflammatory effects of IL-10 during human endotoxemia. J Immunol 2000; 165:2783-9; PMID:10946310; http://dx.doi.org/10.4049/jimmunol.165.5.2783
   PubMed Web of Science ®Google Scholar
• Holmgaard RB, Zamarin D, Munn DH, Wolchok JD, Allison JP. Indoleamine 2,3-dioxygenase is a critical resistance mechanism in antitumor T cell immunotherapy targeting CTLA-4. J Exp Med 2013; 210:1389-402; PMID:23752227; http://dx.doi.org/10.1084/jem.20130066
   PubMed Web of Science ®Google Scholar