Sub-lethal irradiation of human colorectal tumor cells imparts enhanced and sustained susceptibility to multiple death receptor signaling pathways

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Ifeadi, Victoria ^a   Garnett Benson, Charlie ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEATH RECEPTOR; DEATH RECEPTOR 4; DEATH RECEPTOR 5; FAS ANTIGEN; FLICE INHIBITORY PROTEIN; LYMPHOTOXIN BETA RECEPTOR; PROTEIN BCL XL; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED DEATH DOMAIN PROTEIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR;

APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL SURFACE; COLORECTAL TUMOR; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IONIZING RADIATION; PROTEIN EXPRESSION; RADIOSENSITIVITY; TUMOR CELL; CELL STRAIN HCT116; DRUG EFFECT; FLOW CYTOMETRY; GENETICS; METABOLISM; RADIATION EXPOSURE; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANTIGENS, CD95; BLOTTING, WESTERN; CELL PROLIFERATION; COLORECTAL NEOPLASMS; FLOW CYTOMETRY; HCT116 CELLS; HUMANS; RADIATION, IONIZING; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED DEATH DOMAIN PROTEIN; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84857542033     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031762     Document Type: Article

References (76)

1. Kufe D, Weichselbaum R, (2003) Radiation therapy: activation for gene transcription and the development of genetic radiotherapy-therapeutic strategies in oncology. Cancer Biol Ther 2: 326-329.
2. Formenti SC, Demaria S, (2008) Effects of chemoradiation on tumor-host interactions: the immunologic side. J Clin Oncol 26: 1562-1563 author reply 1563.
3. Decker RH, Wilson LD, (2008) Postoperative radiation therapy for non-small cell lung cancer. Semin Thorac Cardiovasc Surg 20: 184-187.
4. Hodge JW, Guha C, Neefjes J, Gulley JL, (2008) Synergizing radiation therapy and immunotherapy for curing incurable cancers. Opportunities and challenges. Oncology (Williston Park) 22: 1064-1070 discussion 1075, 1080-1061, 1084.
5. Guyot F, Faivre J, Manfredi S, Meny B, Bonithon-Kopp C, et al. (2005) Time trends in the treatment and survival of recurrences from colorectal cancer. Ann Oncol 16: 756-761.
6. Kopetz S, Abbruzzese JL, (2009) Barriers to Integrating Gene Profiling for Stage II Colon Cancer. Clin Cancer Res 15: 7451-7452.
7. Ferrara TA, Hodge JW, Gulley JL, (2009) Combining radiation and immunotherapy for synergistic antitumor therapy. Curr Opin Mol Ther 11: 37-42.
8. Sharp HJ, Wansley EK, Garnett CT, Chakraborty M, Camphausen K, et al. (2007) Synergistic antitumor activity of immune strategies combined with radiation. Front Biosci 12: 4900-4910.
9. Friedman EJ, (2002) Immune modulation by ionizing radiation and its implications for cancer immunotherapy. Curr Pharm Des 8: 1765-1780.
10. Chakraborty M, Abrams SI, Camphausen K, Liu K, Scott T, et al. (2003) Irradiation of tumor cells up-regulates Fas and enhances CTL lytic activity and CTL adoptive immunotherapy. J Immunol 170: 6338-6347.
11. Demaria S, Kawashima N, Yang AM, Devitt ML, Babb JS, et al. (2005) Immune-mediated inhibition of metastases after treatment with local radiation and CTLA-4 blockade in a mouse model of breast cancer. Clin Cancer Res 11: 728-734.
12. Nesslinger NJ, Sahota RA, Stone B, Johnson K, Chima N, et al. (2007) Standard treatments induce antigen-specific immune responses in prostate cancer. Clin Cancer Res 13: 1493-1502.
13. Chi KH, Liu SJ, Li CP, Kuo HP, Wang YS, et al. (2005) Combination of conformal radiotherapy and intratumoral injection of adoptive dendritic cell immunotherapy in refractory hepatoma. J Immunother 28: 129-135.
14. Demaria S, Ng B, Devitt ML, Babb JS, Kawashima N, et al. (2004) Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated. Int J Radiat Oncol Biol Phys 58: 862-870.
15. Lugade AA, Moran JP, Gerber SA, Rose RC, Frelinger JG, et al. (2005) Local radiation therapy of B16 melanoma tumors increases the generation of tumor antigen-specific effector cells that traffic to the tumor. J Immunol 174: 7516-7523.
16. Lugade AA, Sorensen EW, Gerber SA, Moran JP, Frelinger JG, et al. (2008) Radiation-induced IFN-gamma production within the tumor microenvironment influences antitumor immunity. J Immunol 180: 3132-3139.
17. Demaria S, Bhardwaj N, McBride WH, Formenti SC, (2005) Combining radiotherapy and immunotherapy: a revived partnership. Int J Radiat Oncol Biol Phys 63: 655-666.
18. Dunn GP, Old LJ, Schreiber RD, (2004) The immunobiology of cancer immunosurveillance and immunoediting. Immunity 21: 137-148.
19. Blattman J, Greenberg P, (2004) Cancer immunotherapy: a treatment for the masses. Science 305: 200-205.
20. Hoos A, Ibrahim R, Korman A, Abdallah K, Berman D, et al. (2010) Development of ipilimumab: contribution to a new paradigm for cancer immunotherapy. Semin Oncol 37: 533-546.
21. Vergati M, Intrivici C, Huen NY, Schlom J, Tsang KY, (2010) Strategies for cancer vaccine development. J Biomed Biotechnol.
22. Whelan M, Whelan J, Russell N, Dalgleish A, (2003) Cancer immunotherapy: an embarrassment of riches? Drug Discov Today 8: 253-258.
23. Antonia S, Mule JJ, Weber JS, (2004) Current developments of immunotherapy in the clinic. Curr Opin Immunol 16: 130-136.
24. Gulley JL, Arlen PM, Bastian A, Morin S, Marte J, et al. (2005) Combining a recombinant cancer vaccine with standard definitive radiotherapy in patients with localized prostate cancer. Clin Cancer Res 11: 3353-3362.
25. Lechleider RJ, Arlen PM, Tsang KY, Steinberg SM, Yokokawa J, et al. (2008) Safety and immunologic response of a viral vaccine to prostate-specific antigen in combination with radiation therapy when metronomic-dose interleukin 2 is used as an adjuvant. Clin Cancer Res 14: 5284-5291.
26. Dudley ME, Yang JC, Sherry R, Hughes MS, Royal R, et al. (2008) Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol 26: 5233-5239.
27. Houghton JA, Harwood FG, Tillman DM, (1997) Thymineless death in colon carcinoma cells is mediated via fas signaling. Proc Natl Acad Sci U S A 94: 8144-8149.
28. Thorburn A, (2004) Death receptor-induced cell killing. Cell Signal 16: 139-144.
29. Aggarwal S, Gollapudi S, Yel L, Gupta AS, Gupta S, (2000) TNF-alpha-induced apoptosis in neonatal lymphocytes: TNFRp55 expression and downstream pathways of apoptosis. Genes Immun 1: 271-279.
30. Baud V, Karin M, (2001) Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol 11: 372-377.
31. Lukashev M, LePage D, Wilson C, Bailly V, Garber E, et al. (2006) Targeting the lymphotoxin-beta receptor with agonist antibodies as a potential cancer therapy. Cancer research 66: 9617-9624.
32. Yang D, Ud Din N, Browning DD, Abrams SI, Liu K, (2007) Targeting lymphotoxin beta receptor with tumor-specific T lymphocytes for tumor regression. Clinical cancer research: an official journal of the American Association for Cancer Research 13: 5202-5210.
33. Dunn GP, Old LJ, Schreiber RD, (2004) The three Es of cancer immunoediting. Annu Rev Immunol 22: 329-360.
34. Garnett CT, Palena C, Chakraborty M, Tsang KY, Schlom J, et al. (2004) Sublethal irradiation of human tumor cells modulates phenotype resulting in enhanced killing by cytotoxic T lymphocytes. Cancer Res 64: 7985-7994.
35. Gelbard A, Garnett CT, Abrams SI, Patel V, Gutkind JS, et al. (2006) Combination chemotherapy and radiation of human squamous cell carcinoma of the head and neck augments CTL-mediated lysis. Clin Cancer Res 12: 1897-1905.
36. Ashkenazi A, (2008) Targeting the extrinsic apoptosis pathway in cancer. Cytokine Growth Factor Rev 19: 325-331.
37. Ashkenazi A, Holland P, Eckhardt SG, (2008) Ligand-based targeting of apoptosis in cancer: the potential of recombinant human apoptosis ligand 2/Tumor necrosis factor-related apoptosis-inducing ligand (rhApo2L/TRAIL). J Clin Oncol 26: 3621-3630.
38. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, et al. (1999) Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 5: 157-163.
39. Jin Z, El-Deiry WS, (2005) Overview of cell death signaling pathways. Cancer Biol Ther 4: 139-163.
40. White-Gilbertson S, Mullen T, Senkal C, Lu P, Ogretmen B, et al. (2009) Ceramide synthase 6 modulates TRAIL sensitivity and nuclear translocation of active caspase-3 in colon cancer cells. Oncogene 28: 1132-1141.
41. Liu F, Hu X, Zimmerman M, Waller JL, Wu P, et al. (2011) TNFalpha cooperates with IFN-gamma to repress Bcl-xL expression to sensitize metastatic colon carcinoma cells to TRAIL-mediated apoptosis. PloS one 6: e16241.
42. Xu J, Zhou JY, Wei WZ, Wu GS, (2010) Activation of the Akt survival pathway contributes to TRAIL resistance in cancer cells. PloS one 5: e10226.
43. Rosato RR, Almenara JA, Coe S, Grant S, (2007) The multikinase inhibitor sorafenib potentiates TRAIL lethality in human leukemia cells in association with Mcl-1 and cFLIPL down-regulation. Cancer Res 67: 9490-9500.
44. Shankar S, Singh TR, Srivastava RK, (2004) Ionizing radiation enhances the therapeutic potential of TRAIL in prostate cancer in vitro and in vivo: Intracellular mechanisms. Prostate 61: 35-49.
45. Voelkel-Johnson C, Hannun YA, El-Zawahry A, (2005) Resistance to TRAIL is associated with defects in ceramide signaling that can be overcome by exogenous C6-ceramide without requiring down-regulation of cellular FLICE inhibitory protein. Mol Cancer Ther 4: 1320-1327.
46. Ogasawara J, Watanabe-Fukunaga R, Adachi M, Matsuzawa A, Kasugai T, et al. (1993) Lethal effect of the anti-Fas antibody in mice. Nature 364: 806-809.
47. Strater J, Hinz U, Hasel C, Bhanot U, Mechtersheimer G, et al. (2005) Impaired CD95 expression predisposes for recurrence in curatively resected colon carcinoma: clinical evidence for immunoselection and CD95L mediated control of minimal residual disease. Gut 54: 661-665.
48. Sheard MA, Uldrijan S, Vojtesek B, (2003) Role of p53 in regulating constitutive and X-radiation-inducible CD95 expression and function in carcinoma cells. Cancer Res 63: 7176-7184.
49. Huerta S, Heinzerling JH, Anguiano-Hernandez YM, Huerta-Yepez S, Lin J, et al. (2007) Modification of gene products involved in resistance to apoptosis in metastatic colon cancer cells: roles of Fas, Apaf-1, NFkappaB, IAPs, Smac/DIABLO, and AIF. The Journal of surgical research 142: 184-194.
50. Chakraborty M, Abrams SI, Coleman CN, Camphausen K, Schlom J, et al. (2004) External beam radiation of tumors alters phenotype of tumor cells to render them susceptible to vaccine-mediated T-cell killing. Cancer Res 64: 4328-4337.
51. Sheard MA, Vojtesek B, Janakova L, Kovarik J, Zaloudik J, (1997) Up-regulation of Fas (CD95) in human p53wild-type cancer cells treated with ionizing radiation. Int J Cancer 73: 757-762.
52. Sheard MA, Krammer PH, Zaloudik J, (1999) Fractionated gamma-irradiation renders tumour cells more responsive to apoptotic signals through CD95. Br J Cancer 80: 1689-1696.
53. Rigberg DA, Centeno J, Kim FS, Ke B, Swenson K, et al. (1999) Irradiation-induced up-regulation of Fas in esophageal squamous cell carcinoma is not accompanied by Fas ligand-mediated apoptosis. J Surg Oncol 71: 91-96.
54. Chakraborty M, Wansley EK, Carrasquillo JA, Yu S, Paik CH, et al. (2008) The use of chelated radionuclide (samarium-153-ethylenediaminetetramethylenephosphonate) to modulate phenotype of tumor cells and enhance T cell-mediated killing. Clin Cancer Res 14: 4241-4249.
55. Takamizawa S, Okamoto S, Bishop W, Wen J, Kimura K, et al. (2000) Differential apoptosis gene expression in pediatric tumors of the kidney. J Pediatr Surg 35: 390-395.
56. Luce A, Courtin A, Levalois C, Altmeyer-Morel S, Romeo PH, et al. (2009) Death receptor pathways mediate targeted and non-targeted effects of ionizing radiations in breast cancer cells. Carcinogenesis 30: 432-439.
57. Hamasu T, Inanami O, Asanuma T, Kuwabara M, (2005) Enhanced induction of apoptosis by combined treatment of human carcinoma cells with X rays and death receptor agonists. J Radiat Res (Tokyo) 46: 103-110.
58. Marini P, Schmid A, Jendrossek V, Faltin H, Daniel PT, et al. (2005) Irradiation specifically sensitises solid tumour cell lines to TRAIL mediated apoptosis. BMC Cancer 5: 5.
59. Niyazi M, Marini P, Daniel PT, Humphreys R, Jendrossek V, et al. (2009) Efficacy of triple therapies including ionising radiation, agonistic TRAIL antibodies and cisplatin. Oncol Rep 21: 1455-1460.
60. Verbrugge I, Wissink EH, Rooswinkel RW, Jongsma J, Beltraminelli N, et al. (2009) Combining radiotherapy with APO010 in cancer treatment. Clin Cancer Res 15: 2031-2038.
61. Ware CF, (2005) Network communications: lymphotoxins, LIGHT, and TNF. Annual review of immunology 23: 787-819.
62. Aggarwal BB, (2003) Signalling pathways of the TNF superfamily: a double-edged sword. Nature reviews Immunology 3: 745-756.
63. Mauri DN, Ebner R, Montgomery RI, Kochel KD, Cheung TC, et al. (1998) LIGHT, a new member of the TNF superfamily, and lymphotoxin alpha are ligands for herpesvirus entry mediator. Immunity 8: 21-30.
64. Kimura K, Gelmann EP, (2000) Tumor necrosis factor-alpha and Fas activate complementary Fas-associated death domain-dependent pathways that enhance apoptosis induced by gamma-irradiation. J Biol Chem 275: 8610-8617.
65. Chen MC, Hwang MJ, Chou YC, Chen WH, Cheng G, et al. (2003) The role of apoptosis signal-regulating kinase 1 in lymphotoxin-beta receptor-mediated cell death. The Journal of biological chemistry 278: 16073-16081.
66. Andersen MH, Becker JC, Straten P, (2005) Regulators of apoptosis: suitable targets for immune therapy of cancer. Nat Rev Drug Discov 4: 399-409.
67. Johnstone RW, Ruefli AA, Lowe SW, (2002) Apoptosis: a link between cancer genetics and chemotherapy. Cell 108: 153-164.
68. Tschopp J, Irmler M, Thome M, (1998) Inhibition of fas death signals by FLIPs. Curr Opin Immunol 10: 552-558.
69. Kataoka T, Schroter M, Hahne M, Schneider P, Irmler M, et al. (1998) FLIP prevents apoptosis induced by death receptors but not by perforin/granzyme B, chemotherapeutic drugs, and gamma irradiation. J Immunol 161: 3936-3942.
70. Scaffidi C, Schmitz I, Zha J, Korsmeyer SJ, Krammer PH, et al. (1999) Differential modulation of apoptosis sensitivity in CD95 type I and type II cells. J Biol Chem 274: 22532-22538.
71. Ravi R, Bedi A, (2002) Sensitization of tumor cells to Apo2 ligand/TRAIL-induced apoptosis by inhibition of casein kinase II. Cancer research 62: 4180-4185.
72. LeBlanc H, Lawrence D, Varfolomeev E, Totpal K, Morlan J, et al. (2002) Tumor-cell resistance to death receptor-induced apoptosis through mutational inactivation of the proapoptotic Bcl-2 homolog Bax. Nat Med 8: 274-281.
73. Yang A, Wilson NS, Ashkenazi A, (2010) Proapoptotic DR4 and DR5 signaling in cancer cells: toward clinical translation. Curr Opin Cell Biol 22: 837-844.
74. Shibue T, Suzuki S, Okamoto H, Yoshida H, Ohba Y, et al. (2006) Differential contribution of Puma and Noxa in dual regulation of p53-mediated apoptotic pathways. Embo J 25: 4952-4962.
75. Nawrocki ST, Carew JS, Douglas L, Cleveland JL, Humphreys R, et al. (2007) Histone deacetylase inhibitors enhance lexatumumab-induced apoptosis via a p21Cip1-dependent decrease in survivin levels. Cancer research 67: 6987-6994.
76. Wang H, Gao X, Huang Y, Yang J, Liu ZR, (2009) P68 RNA helicase is a nucleocytoplasmic shuttling protein. Cell research 19: 1388-1400.