Inflammatory cytokines IL-17 and TNF-α up-regulate PD-L1 expression in human prostate and colon cancer cells - PubMed
Inflammatory cytokines IL-17 and TNF-α up-regulate PD-L1 expression in human prostate and colon cancer cells
Xun Wang et al. Immunol Lett. 2017 Apr.
Abstract
Programmed cell death protein 1 (PD-1) acts on PD-1 ligands (PD-L1 and PD-L2) to suppress activation of cytotoxic T lymphocytes. Interleukin-17 (IL-17) and tumor necrosis factor-α (TNF-α) are co-expressed by T helper 17 (TH17) cells in many tumors. The purpose of this study was to test if IL-17 and TNF-α may synergistically induce PD-L1 expression in human prostate cancer LNCaP and human colon cancer HCT116 cell lines. We found that IL-17 did not induce PD-L1 mRNA expression, but up-regulated PD-L1 protein expression in HCT116 and LNCaP cells. TNF-α induced PD-L1 mRNA and protein expression in both cell lines. Neither IL-17 nor TNF-α induced PD-L2 mRNA or protein expression. IL-17 and TNF-α acted individually rather than cooperatively in induction of PD-L1 expression. IL-17 and/or TNF-α activated AKT, nuclear factor-κB (NF-κB), and extracellular signal-regulated kinases 1/2 (ERK1/2) signaling pathways in HCT116 cells, whereas only NF-κB signaling was activated in LNCaP cells. NF-κB inhibitor could diminish PD-L1 protein expression induced by IL-17 and/or TNF-α in both HCT116 and LNCaP cell lines. ERK1/2 inhibitor could also reduce PD-L1 protein expression induced by IL-17 and/or TNF-α in HCT116 cells, while AKT inhibitor could abolish PD-L1 protein expression induced by IL-17 and/or TNF-α in LNCaP cells. These results suggest that IL-17 and TNF-α act individually rather than cooperatively through activation of NF-κB and ERK1/2 signaling to up-regulate PD-L1 expression in HCT116 cells, while the two inflammatory cytokines act through activation of NF-κB signaling, in the presence of AKT activity, to up-regulate PD-L1 expression in LNCaP cells.
Keywords: Colon cancer; Interleukin-17; Programmed cell death protein 1 ligand 1; Prostate cancer; Tumor necrosis factor-α.
Copyright © 2017 European Federation of Immunological Societies. Published by Elsevier B.V. All rights reserved.
Conflict of interest statement
Conflicts of interest
The authors declare no conflicts of interest.
Figures

Effects of IL-17 and/or TNF-α on PD-L1 and PD-L2 mRNA expression in human cancer cell lines HCT116 and LNCaP. (A and B) The cells were treated with IL-17 (20 ng/ml), TNF-α (10 ng/ml), or a combination of both for 3 hours. PD-L1 and PD-L2 mRNA expression was determined by qRT-PCR analysis. Data were represented as means ± SD (error bars) of three independent experiments.

Effects of IL-17 and/or TNF-α on PD-L1 and PD-L2 protein expression in human cancer cell lines HCT116 and LNCaP. (A to C) HCT116 cells and (D to F) LNCaP cells were treated with IL-17 (20 ng/ml), TNF-α (10 ng/ml), or a combination of both for the indicated time. PD-L1 and PD-L2 protein expression was analyzed using Western blot analysis. GAPDH was probed for protein loading control (A and D). The relative protein levels were presented as the ratio of PD-L1/GAPDH or PD-L2/GAPDH (B–C and E–F), which was normalized against the ratio of the control group (arbitrarily designated as “1”). Data were represented as means ± SD of three independent experiments.

Effects of IL-17 and/or TNF-α on activation of signaling pathways in human colon cancer line HCT116. (A to H) HCT116 cells were treated with IL-17 (20 ng/ml), TNF-α (10 ng/ml), or a combination of both for the indicated time. Activation of Akt, IκBα, and ERK1/2 was assessed using Western blot analysis. GAPDH was probed for protein loading control (A and B). Relative protein levels were presented as the ratio of each protein divided by GAPDH, which was normalized against the ratio of the control group (arbitrarily designated as “1”) (C to H). Data were represented as means ± SD of three independent experiments.

Effects of IL-17 and/or TNF-α on activation of signaling pathways in human prostate cancer line LNCaP. (A to E) LNCaP cells were treated with IL-17 (20 ng/ml), TNF-α (10 ng/ml), or a combination of both for the indicated time. Activation of Akt, IκBα, and ERK1/2 was assessed using Western blot analysis. GAPDH was probed for protein loading control (A). Relative protein levels were presented as the ratio of each protein divided by GAPDH, which was normalized against the ratio of the control group (arbitrarily designated as “1”) (B to E). Data were represented as means ± SD of three independent experiments.

Effects of pan-Akt inhibitor (AZD5363), MEK/ERK1/2 inhibitor (U0126), and NF-κB inhibitor (Bay11-7082) on PD-L1 protein expression induced by IL-17 and/or TNF-α in human cancer cell lines HCT116 and LNCaP. (A and C) HCT116 cells and (B and D) LNCaP cells were first treated with AZD5363 (2 μM), U0126 (10 μM), or Bay11-7082 (5 μM) for 30 minutes. Then, HCT116 cells were treated with IL-17 (20 ng/ml), TNF-α (10 ng/ml), or a combination of both for 24 hours, while LNCaP cells were similarly treated for 8 hours. PD-L1 protein levels were analyzed using Western blot analysis. GAPDH was probed for protein loading control (A and B). Relative protein levels were presented as the ratio of PD-L1/GAPDH, which was normalized against the ratio of the control group (arbitrarily designated as “1”) (C and D). Data were represented as means ± SD of three independent experiments. *P< 0.05 and **P< 0.01, compared to the corresponding group with IL-17 and/or TNF-α treatment in the absence of any inhibitor.
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References
-
- Fitzmaurice C, Dicker D, Pain A, Hamavid H, Moradi-Lakeh M, MacIntyre MF, Allen C, Hansen G, Woodbrook R, Wolfe C, Hamadeh RR, Moore A, Werdecker A, Gessner BD, Te Ao B, McMahon B, Karimkhani C, Yu C, Cooke GS, Schwebel DC, Carpenter DO, Pereira DM, Nash D, Kazi DS, De Leo D, Plass D, Ukwaja KN, Thurston GD, Yun Jin K, Simard EP, Mills E, Park EK, Catala-Lopez F, deVeber G, Gotay C, Khan G, Hosgood HD, 3rd, Santos IS, Leasher JL, Singh J, Leigh J, Jonas JB, Sanabria J, Beardsley J, Jacobsen KH, Takahashi K, Franklin RC, Ronfani L, Montico M, Naldi L, Tonelli M, Geleijnse J, Petzold M, Shrime MG, Younis M, Yonemoto N, Breitborde N, Yip P, Pourmalek F, Lotufo PA, Esteghamati A, Hankey GJ, Ali R, Lunevicius R, Malekzadeh R, Dellavalle R, Weintraub R, Lucas R, Hay R, Rojas-Rueda D, Westerman R, Sepanlou SG, Nolte S, Patten S, Weichenthal S, Abera SF, Fereshtehnejad SM, Shiue I, Driscoll T, Vasankari T, Alsharif U, Rahimi-Movaghar V, Vlassov VV, Marcenes WS, Mekonnen W, Melaku YA, Yano Y, Artaman A, Campos I, MacLachlan J, Mueller U, Kim D, Trillini M, Eshrati B, Williams HC, Shibuya K, Dandona R, Murthy K, Cowie B, Amare AT, Antonio CA, Castaneda-Orjuela C, van Gool CH, Violante F, Oh IH, Deribe K, Soreide K, Knibbs L, Kereselidze M, Green M, Cardenas R, Roy N, Tillmann T, Li Y, Krueger H, Monasta L, Dey S, Sheikhbahaei S, Hafezi-Nejad N, Kumar GA, Sreeramareddy CT, Dandona L, Wang H, Vollset SE, Mokdad A, Salomon JA, Lozano R, Vos T, Forouzanfar M, Lopez A, Murray C, Naghavi M. The Global Burden of Cancer 2013. JAMA Oncol. 2015;1:505–527. - PMC - PubMed
-
- Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K, Pitot HC, Hamid O, Bhatia S, Martins R, Eaton K, Chen S, Salay TM, Alaparthy S, Grosso JF, Korman AJ, Parker SM, Agrawal S, Goldberg SM, Pardoll DM, Gupta A, Wigginton JM. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med. 2012;366:2455–2465. - PMC - PubMed
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