DOI QR코드

DOI QR Code

Induction of Indoleamine 2,3-dioxygenase (IDO) Enzymatic Activity Contributes to Interferon-Gamma Induced Apoptosis and Death Receptor 5 Expression in Human Non-small Cell Lung Cancer Cells

  • Chung, Ting Wen (Division of Chest Medicine, Department of Internal Medicine, Changhua Christian Hospital) ;
  • Tan, Kok-Tong (Tungs' Taichung MetroHarbor Hospital) ;
  • Chan, Hong-Lin (Institute of Bioinformatics and Structural Biology and Department of Medical Sciences, National Tsing Hua University) ;
  • Lai, Ming-Derg (Department of Biochemistry and Molecular Biology, National Cheng-Kung University) ;
  • Yen, Meng-Chi (Department of Biochemistry and Molecular Biology, National Cheng-Kung University) ;
  • Li, Yi-Ron (Institute of Biomedical Sciences, College of Life Science, National Chung Hsing University) ;
  • Lin, Sheng Hao (Division of Chest Medicine, Department of Internal Medicine, Changhua Christian Hospital) ;
  • Lin, Chi-Chen (Division of Chest Medicine, Department of Internal Medicine, Changhua Christian Hospital)
  • Published : 2014.10.11

Abstract

Interferon-gamma (IFN-${\gamma}$) has been used to treat various malignant tumors. However, the molecular mechanisms underlying the direct anti-proliferative activity of IFN-${\gamma}$ are poorly understood. In the present study, we examined the in vitro antitumor activity of IFN-${\gamma}$ on two human non-small-cell lung carcinoma (NSCLC) cell lines, H322M and H226. Our findings indicated that IFN-${\gamma}$ treatment caused a time-dependent reduction in cell viability and induced apoptosis through a FADD-mediated caspase-8/tBid/mitochondria-dependent pathway in both cell lines. Notably, we also postulated that IFN-${\gamma}$ increased indoleamine 2,3-dioxygenase (IDO) expression and enzymatic activity in H322M and H226 cells. In addition, inhibition of IDO activity by the IDO inhibitor 1-MT or tryptophan significantly reduced IFN-${\gamma}$-induced apoptosis and death receptor 5 (DR5) expression, which suggests that IDO enzymatic activity plays an important role in the anti-NSCLC cancer effect of IFN-${\gamma}$. These results provide new mechanistic insights into interferon-${\gamma}$ antitumor activity and further support IFN-${\gamma}$ as a potential therapeutic adjuvant for the treatment of NCSLC.

References

  1. Chon SY, Hassanain HH, Gupta SL (1996). Cooperative role of interferon regulatory factor 1 and p91 (stat1) response elements in interferon-gamma-inducible expression of human indoleamine 2,3-dioxygenase gene. J Biol Chem, 271, 17247-52. https://doi.org/10.1074/jbc.271.29.17247
  2. Bray F, Cancer, I.A.f.R.o (2014). Globocan 2012: Estimated cancer incidence, mortality and prevalence worldwide in 2012.
  3. Chen J, Hou J, Zhang J, et al (2012) Atorvastatin synergizes with IFN-$\gamma$ in treating human non-small cell lung carcinomas via potent inhibition of RhoA activity. Eur J Pharmacol, 682, 161-70 https://doi.org/10.1016/j.ejphar.2012.02.015
  4. Chen SC, Lin YL, Huang B, (2011) Salvianolic acid B suppresses IFN-$\gamma$-induced JAK/STAT1 activation in endothelial cells. Thromb Res,128, 560-4 https://doi.org/10.1016/j.thromres.2011.08.032
  5. de la Maza LM, Peterson EM (1988). Dependence of the in vitro antiproliferative activity of recombinant human gammainterferon on the concentration of tryptophan in culture media. Cancer Res, 48, 346-50.
  6. Fallarino F, Grohmann U, Vacca C, et al (2002). T cell apoptosis by tryptophan catabolism. Cell Death Differ, 9, 1069-77. https://doi.org/10.1038/sj.cdd.4401073
  7. Fujigaki H, Seishima M, K Saito (2012). Posttranslational modification of indoleamine 2,3-dioxygenase. Anal Bioanal Chem, 403, 1777-82. https://doi.org/10.1007/s00216-012-5946-2
  8. Guo Y, Wang G, Gao WW et al (2012) Induction of apoptosis in glioma cells and upregulation of Fas expression using the human interferon-$\beta$ gene. Asian Pac J Cancer Prev, 13, 2837-40 https://doi.org/10.7314/APJCP.2012.13.6.2837
  9. Hong S, Kim HY, Kim J, et al (2013). Smad7 protein induces interferon regulatory factor 1-dependent transcriptional activation of caspase 8 to restore tumor necrosis factorrelated apoptosis-inducing ligand (trail)-mediated apoptosis. J Biol Chem, 288, 3560-70. https://doi.org/10.1074/jbc.M112.400408
  10. Hagiwara K, Kobayashi K (2013). Importance of the cytological samples for the epidermal growth factor receptor gene mutation test for non-small cell lung cancer. Cancer science, 104, 291-7. https://doi.org/10.1111/cas.12081
  11. Hayakawa Y, Sato-Matsushita M, Takeda K, et al (2011). Early activation and interferon-$\gamma$ production of tumor-infiltrating mature cd27high natural killer cells. Cancer science, 102, 1967-71. https://doi.org/10.1111/j.1349-7006.2011.02042.x
  12. Hong M, Jiang Z, Zhou YF (2014). Effects of thermotherapy on th1/th2 cells in esophageal cancer patients treated with radiotherapy. Asian Pac J Cancer Prev, 15, 2359. https://doi.org/10.7314/APJCP.2014.15.5.2359
  13. Hou W, Huang G, Cao X, (2014) Suppression of experimental autoimmune glomerulonephritis by tryptophan. J Nephrol, 27, 19-28. https://doi.org/10.1007/s40620-013-0020-5
  14. Jin CG, Chen XQ, Li J, et al (2013). Moderating effects and maintenance of lung cancer cellular immune functions by CIK cell therapy. Asian Pac J Cancer Prev, 14, 3587-92. https://doi.org/10.7314/APJCP.2013.14.6.3587
  15. Kluck RM, Bossy-Wetzel E, Green DR, et al (1997). The release of cytochrome c from mitochondria: A primary site for bcl-2 regulation of apoptosis. Science, 275, 1132-6. https://doi.org/10.1126/science.275.5303.1132
  16. Lee GK, Park HJ, Macleod M, et al (2002). Tryptophan deprivation sensitizes activated t cells to apoptosis prior to cell division. Immunology, 107, 452-60. https://doi.org/10.1046/j.1365-2567.2002.01526.x
  17. Lee SM, Lee YS, Choi JH, et al (2010) Tryptophan metabolite 3-hydroxyanthranilic acid selectively induces activated T cell death via intracellular GSH depletion. Immunol Lett, 132, 53-60 https://doi.org/10.1016/j.imlet.2010.05.008
  18. Mailankot M, Nagaraj RH (2010). Induction of indoleamine 2,3-dioxygenase by interferon-gamma in human lens epithelial cells: Apoptosis through the formation of 3-hydroxykynurenine. Int J Biochem Cell Biol, 42, 1446-54. https://doi.org/10.1016/j.biocel.2010.04.014
  19. Li H, Zhu H, Xu CJ, et al (1998). Cleavage of bid by caspase 8 mediates the mitochondrial damage in the fas pathway of apoptosis. Cell, 94, 491-501. https://doi.org/10.1016/S0092-8674(00)81590-1
  20. Li Y, Tredget EE, Ghahary A (2004). Cell surface expression of mhc class i antigen is suppressed in indoleamine 2,3-dioxygenase genetically modified keratinocytes: Implications in allogeneic skin substitute engraftment. Hum Immunol, 65, 114-23. https://doi.org/10.1016/j.humimm.2003.11.004
  21. Liu RY, Zhu YH, Zhou L, et al (2012) Adenovirus-mediated delivery of interferon-$\gamma$ gene inhibits the growth of nasopharyngeal carcinoma. J Transl Med. 10, 256. https://doi.org/10.1186/1479-5876-10-256
  22. Mailankot M, Staniszewska MM, Butler H, et al (2009). Indoleamine 2,3-dioxygenase overexpression causes kynurenine-modification of proteins, fiber cell apoptosis and cataract formation in the mouse lens. Lab Invest, 89, 498-512. https://doi.org/10.1038/labinvest.2009.22
  23. Mitsudomi T (2010). Advances in target therapy for lung cancer. Jpn J Clin Oncol, 40, 101-6. https://doi.org/10.1093/jjco/hyp174
  24. Morita T, Saito K, Takemura M, et al (2001). 3-hydroxyanthranilic acid, an l-tryptophan metabolite, induces apoptosis in monocyte-derived cells stimulated by interferon-gamma. Ann Clin Biochem, 38, 242-51. https://doi.org/10.1258/0004563011900461
  25. Ozaki Y, Edelstein MP, Duch DS (1988). Induction of indoleamine 2,3-dioxygenase: A mechanism of the antitumor activity of interferon gamma. Proc Natl Acad Sci U S A, 85, 1242-6. https://doi.org/10.1073/pnas.85.4.1242
  26. Platten M, Wick W and Van den Eynde BJ. Tryptophan catabolism in cancer: beyond IDO and tryptophan depletion. Cancer Res. 72, 5435-40.
  27. Satoh A, Toyota M, Ikeda H, et al (2004). Epigenetic inactivation of class ii transactivator (ciita) is associated with the absence of interferon-gamma-induced hla-dr expression in colorectal and gastric cancer cells. Oncogene, 23, 8876-86. https://doi.org/10.1038/sj.onc.1208144
  28. Prior C, Oroszy S, Oberaigner W, et al (1999). Advanced non-small-cell lung cancer: Adjunctive interferon gamma in induction and maintenance therapy. J Cancer Res Clin Oncol, 125, 42-6. https://doi.org/10.1007/s004320050240
  29. Sagan D, Kocki T, Kocki J, et al (2012). Serum kynurenic acid: Possible association with invasiveness of non-small cell lung cancer. Asian Pac J Cancer Prev, 13, 4241-4. https://doi.org/10.7314/APJCP.2012.13.9.4741
  30. Sankari SL, Masthan K, Babu NA, et al (2012). Apoptosis in cancer -an update. Asian Pac J Cancer Prev, 13, 4873-78. https://doi.org/10.7314/APJCP.2012.13.10.4873
  31. Smiley ST, Reers M, Mottola-Hartshorn C, et al (1991). Intracellular heterogeneity in mitochondrial membrane potentials revealed by a j-aggregate-forming lipophilic cation jc-1. Proc Natl Acad Sci U S A, 88, 3671-5. https://doi.org/10.1073/pnas.88.9.3671
  32. Sun DS, Hu LK, Cai Y, et al (2014). A systematic review of risk factors for brain metastases and value of prophylactic cranial irradiation in non-small cell lung cancer. Asian Pac J Cancer Prev, 15, 1233-9 https://doi.org/10.7314/APJCP.2014.15.3.1233
  33. Song H, Park H, Kim YS, et al (2011). L-kynurenine-induced apoptosis in human nk cells is mediated by reactive oxygen species. Int Immunopharmacol, 11, 932-8. https://doi.org/10.1016/j.intimp.2011.02.005
  34. Sun J, Yu J, Li H, et al (2011). Upregulated expression of indoleamine 2, 3-dioxygenase in cho cells induces apoptosis of competent t cells and increases proportion of treg cells. J Exp Clin Cancer Res, 30, 82. https://doi.org/10.1186/1756-9966-30-82
  35. Surget S, Chiron D, Gomez-Bougie P, et al (2012). Cell death via dr5, but not dr4, is regulated by p53 in myeloma cells. Cancer Res, 72, 4562-73. https://doi.org/10.1158/0008-5472.CAN-12-0487
  36. Wakita D, Chamoto K, Ohkuri T,et al (2009). Ifn-$\gamma$-dependent type 1 immunity is crucial for immunosurveillance against squamous cell carcinoma in a novel mouse carcinogenesis model. Carcinogenesis, 30, 1408-15. https://doi.org/10.1093/carcin/bgp144
  37. Tajima K, Ito Y, Demachi A, et al (2004). Interferon-gamma differentially regulates susceptibility of lung cancer cells to telomerase-specific cytotoxic t lymphocytes. Int J Cancer, 110, 403-12. https://doi.org/10.1002/ijc.20139
  38. Tao Y, Zhang ML, Ma PC, et al (2012). Triptolide inhibits proliferation and induces apoptosis of human melanoma a375 cells. Asian Pac J Cancer Prev, 13, 1611-5. https://doi.org/10.7314/APJCP.2012.13.4.1611
  39. Tate DJ Jr, Patterson JR, Velasco-Gonzalez C, et al (2012) Interferon-gamma-induced nitric oxide inhibits the proliferation of murine renal cellcarcinoma cells. Int J Biol Sci .8, 1109-20 https://doi.org/10.7150/ijbs.4694
  40. Wang F-BW (2014). Interleukin-7 enhances the in vivo antitumor activity of tumor-reactive cd8+ t cells with induction of ifn-gamma in a murine breast cancer model. Asian Pac J Cancer Prev, 15, 265-71. https://doi.org/10.7314/APJCP.2014.15.1.265
  41. Wang N, Wang W, Huo P, et al (2014). Mitochondriamediated apoptosis in human lung cancer a549 cells by 4-methylsulfinyl-3-butenyl isothiocyanate from radish seeds. Asian Pacific journal of cancer prevention: Asian Pac J Cancer Prev, 15, 2133. https://doi.org/10.7314/APJCP.2014.15.5.2133
  42. Xu N, Wu SD, Wang H, et al (2012). Involvement of foxm1 in non-small cell lung cancer recurrence. Asian Pac J Cancer Prev, 13, 4739-43. https://doi.org/10.7314/APJCP.2012.13.9.4739
  43. Yuan CH, Yang XQ, Zhu CL, (2014) Interleukin-7 enhances the in vivo anti-tumor activity of tumor-reactive CD8+ T cells with induction of IFN-gamma in a murine breast cancer model. Asian Pac J Cancer Prev, 15, 265-71 https://doi.org/10.7314/APJCP.2014.15.1.265
  44. Zhao YH , Wang T , Yu GF, et al (2013). Anti-proliferation effects of interferon-gamma on gastric cancer cells. Asian Pac J Cancer Prev, 14, 5513-8. https://doi.org/10.7314/APJCP.2013.14.9.5513
  45. Zheng DJ, Yu GH, Gao JF et al (2013) Concomitant EGFR inhibitors combined with radiation for treatment of non-small cell lung carcinoma. Asian Pac J Cancer Prev, 14, 4485-94 https://doi.org/10.7314/APJCP.2013.14.8.4485

Cited by

  1. Interferon gamma-induced apoptosis of head and neck squamous cell carcinoma is connected to indoleamine-2,3-dioxygenase via mitochondrial and ER stress-associated pathways vol.11, pp.1, 2016, https://doi.org/10.1186/s13008-016-0023-4
  2. Highlights on immune checkpoint inhibitors in non–small cell lung cancer vol.39, pp.3, 2017, https://doi.org/10.1177/1010428317695013