TRAIL recombinant adenovirus triggers robust apoptosis in multidrug-resistant HL-60/Vinc cells preferentially through death receptor DR5

Human Gene Therapy

Volumn 19, Issue 7, 2008, Pages 731-743

  Wu, Ching Huang ^a,b   Kao, Ching Hai ^a,b   Safa, Ahmad R ^a,b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CASPASE 10; CASPASE 3; DEATH RECEPTOR; DEATH RECEPTOR 4; DEATH RECEPTOR 5; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ACUTE GRANULOCYTIC LEUKEMIA; ADENOVIRUS; ADENOVIRUS 5; APOPTOSIS; ARTICLE; CANCER CELL; CELL DEATH; CELL STRAIN HL 60; CONTROLLED STUDY; HUMAN; HUMAN CELL; LYMPHOCYTE; MITOCHONDRIAL MEMBRANE POTENTIAL; MULTIDRUG RESISTANCE; PROTEIN EXPRESSION; RECOMBINANT ADENOVIRUS;

ADENOVIRIDAE; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELLS, CULTURED; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; HL-60 CELLS; HUMANS; LYMPHOCYTES; MEMBRANE POTENTIALS; MITOCHONDRIA; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; RECEPTORS, TUMOR NECROSIS FACTOR; RECOMBINATION, GENETIC;

ADENOVIRIDAE;

EID: 47549090609     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.2008.001     Document Type: Article

References (71)

1. Abedini, M.R., Qiu, Q., Yan, X., and Tsang, B.K. (2004). Possible role of FLICE-like inhibitory protein (FLIP) in chemoresistant ovarian cancer cells in vitro. Oncogene 23, 6997-7004.
2. Ashkenazi, A., Pai, R.C., Fong, S., Leung, S., Lawrence, D.A., Marsters, S.A., Blackie, C., Chang, L., McMurtrey, A.E., Hebert, A., Deforge, L., Koumenis, I.L., Lewis, D., Harris, L., Bussiere, J., Koeppen, H., Shahrokh, Z., and Schwall, R.H. (1999). Safety and antitumor activity of recombinant soluble Apo2 ligand. J. Clin. Invest. 104, 155- 162.
3. Balamotis, M.A., Huang, K., and Mitani, K. (2004). Efficient delivery and stable gene expression in a hematopoietic cell line using a chimeric serotype 35 fiber pseudotyped helper-dependent adenoviral vector. Virology 324, 229-237.
4. Bedi, A., Zehnbauer, B.A., Barber, J.P., Sharkis, S.J., and Jones, R.J. (1994). Inhibition of apoptosis by BCR-ABL in chronic myeloid leukemia. Blood 83, 2038-2044.
5. 2/M transition after DNA damage: A mechanism of resistance to multiple anticancer agents. Blood 86, 1148-1158.
6. Bergelson, J.M., Cunningham, J.A., Droguett, G., Kurt-Jones, E.A., Krithivas, A., Hong, J.S., Horwitz, M.S., Crowell, R.L., and Finberg, R.W. (1997). Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science 275, 1320-1323.
7. Bernt, K.M., Ni, S., Gaggar, A., Li, Z.Y., Shayakhmetov, D.M., and Lieber, A. (2003). The effect of sequestration by nontarget tissues on anti-tumor efficacy of systemically applied, conditionally replicating adenovirus vectors. Mol. Ther. 8, 746-755.
8. L up-regulation. Leukemia 17, 379-389.
9. Bouralexis, S., Findlay, D.M., Atkins, G.J., Labrinidis, A., Hay, S., and Evdokiou, A. (2003). Progressive resistance of BTK-143 osteosarcoma cells to Apo2L/TRAIL-induced apoptosis is mediated by acquisition of DcR2/TRAIL-R4 expression: Resensitisation with chemotherapy. Br. J. Cancer 89, 206-214.
10. Eggert, A., Grotzer, M.A., Zuzak, T.J., Wiewrodt, B.R., Ho, R., Ikegaki, N., and Brodeur, G.M. (2001). Resistance to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis in neuroblastoma cells correlates with a loss of caspase-8 expression. Cancer Res. 61, 1314-1319.
11. Ehrhardt, H., Fulda, S., Schmid, I., Hiscott, J., Debatin, K.M., and Jeremias, I. (2003). TRAIL induced survival and proliferation in cancer cells resistant towards TRAIL-induced apoptosis mediated by NF-κB. Oncogene 22, 3842-3852.
12. Ehtesham, M., Kabos, P., Gutierrez, M.A., Chung, N.H., Griffith, T.S., Black, K.L., and Yu, J.S. (2002). Induction of glioblastoma apoptosis using neural stem cell-mediated delivery of tumor necrosis factor-related apoptosis inducing ligand. Cancer Res. 62, 7170-7174.
13. Gaggar, A., Shayakhmetov, D.M., and Lieber, A. (2003). CD46 is a cellular receptor for group B adenoviruses. Nat. Med. 9, 1408-1412.
14. Gaggar, A., Shayakhmetov, D.M., Liszewski, M.K., Atkinson, J.P., and Lieber, A. (2005). Localization of regions in CD46 that interact with adenovirus. J. Virol. 79, 7503-7513.
15. Green, D.R. (1998). Apoptotic pathways: The roads to ruin. Cell 94, 695-698.
16. Griffith, T.S., Fialkov, J.M., Scott, D.L., Azuhata, T., Williams, R.D., Wall, N.R., Altieri, D.C., and Sandler, A.D. (2002). Induction and regulation of tumor necrosis factor-related apoptosis-inducing ligand/Apo-2 ligand-mediated apoptosis in renal cell carcinoma. Cancer Res. 62, 3093-3099.
17. Gross, A., Yin, X.M., Wang, K., Wei, M.C., Jockel, J., Milliman, C., Erdjument-Bromage, H., Tempst, P., and Korsmeyer, S.J. (1999). Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J. Biol. Chem. 274, 1156-1163.
18. Hao, C., Song, J.H., Hsi, B., Lewis, J., Song, D.K., Petruk, K.C., Tyrrell, D.L., and Kneteman, N.M. (2004). TRAIL inhibits tumor growth but is nontoxic to human hepatocytes in chimeric mice. Cancer Res. 64, 8502-8506.
19. Hasegawa, H., Yamada, Y., Harasawa, H., Tsuji, T., Murata, K., Sugahara, K., Tsuruda, K., Ikeda, S., Imaizumi, Y., Tomonaga, M., Masuda, M., Takasu, N., and Kamihira, S. (2005). Sensitivity of adult T-cell leukaemia lymphoma cells to tumour necrosis factor-related apoptosis-inducing ligand. Br. J. Haematol. 128, 253-265.
20. He, C., Lao, W.F., Hu, X.T., Xu, X.M., Xu, J., and Fang, B.L. (2004). Anti-liver cancer activity of TNF-related apoptosis-inducing ligand gene and its bystander effects. World J. Gastroenterol. 10, 654-659.
21. Huang, M.M., and Hearing, P. (1989). Adenovirus early region 4 encodes two gene products with redundant effects in lytic infection. J. Virol. 63, 2605-2615.
22. Huang, Q., Zhang, X., Wang, H., Yan, B., Kirkpatrick, J., Dewhirst, M.W., and Li, C.Y. (2004). A novel conditionally replicative adenovirus vector targeting telomerase-positive tumor cells. Clin. Cancer Res. 10, 1439-1445.
23. Huang, X., Lin, T., Gu, J., Zhang, L., Roth, J.A., Liu, J., and Fang, B. (2003). Cell to cell contact required for bystander effect of the TNF-related apoptosis inducing ligand (TRAIL) gene. Int. J. Oncol. 22, 1241-1245.
24. Jia, L., Patwari, Y., Kelsey, S.M., and Newland, A.C. (2001). Trail-induced apoptosis in type I leukemic cells is not enhanced by overexpression of Bax. Biochem. Biophys. Res. Commun. 283, 1037-1045.
25. L to death receptor 5. J. Biol. Chem. 279, 55594-55601.
26. Kagawa, S., He, C., Gu, J., Koch, P., Rha, S.J., Roth, J.A., Curley, S.A., Stephens, L.C., and Fang, B. (2001). Antitumor activity and bystander effects of the tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) gene. Cancer Res. 61, 3330-3338.
27. Karacay, B., Sanlioglu, S., Griffith, T.S., Sandler, A., and Bonthius, D.J. (2004). Inhibition of the NF-κB pathway enhances TRAIL-mediated apoptosis in neuroblastoma cells. Cancer Gene Ther. 11, 681-690.
28. Keane, M.M., Rubinstein, Y., Cuello, M., Ettenberg, S.A., Banerjee, P., Nau, M.M., and Lipkowitz, S. (2000). Inhibition of NF-κB activity enhances TRAIL mediated apoptosis in breast cancer cell lines. Breast Cancer Res. Treat. 64, 211-219.
29. Kim, C.Y., Jeong, M., Mushiake, H., Kim, B.M., Kim, W.B., Ko, J.P., Kim, M.H., Kim, M., Kim, T.H., Robbins, P.D., Billiar, T.R., and Seol, D.W. (2006). Cancer gene therapy using a novel secretable trimeric TRAIL. Gene Ther. 13, 330-338.
30. Kim, K., Takimoto, R., Dicker, D.T., Chen, Y., Gazitt, Y., and El-Deiry, W.S. (2001). Enhanced TRAIL sensitivity by p53 overexpression in human cancer but not normal cell lines. Int. J. Oncol. 18, 241-247.
31. L in esophageal squamous cancer to sensitize to chemotherapy plus TRAIL-induced apoptosis while normal epithelial cells are protected by blockade of caspase 9. Cell Death Differ. 11, 583-587.
32. Kim, S.H., Kim, K., Kwagh, J.G., Dicker, D.T., Herlyn, M., Rustgi, A.K., Chen, Y., and El-Deiry, W.S. (2004). Death induction by recombinant native TRAIL and its prevention by a caspase 9 inhibitor in primary human esophageal epithelial cells. J. Biol. Chem. 279, 40044-40052.
33. Li, H., Zhu, H., Xu, C.J., and Yuan, J. (1998). Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94, 491-501.
34. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S.M., Ahmad, M., Alnemri, E.S., and Wang, X. (1997). Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91, 479-489.
35. Li, X., Zhang, Y.P., Kim, H.S., Bae, K.H., Stantz, K.M., Lee, S.J., Jung, C., Jimenez, J.A., Gardner, T.A., Jeng, M.H., and Kao, C. (2005). Gene therapy for prostate cancer by controlling adenovirus E1a and E4 gene expression with PSES enhancer. Cancer Res. 65, 1941-1951.
36. Lichtenstein, D.L., Krajcsi, P., Esteban, D.J., Tollefson, A.E., and Wold, W.S. (2002). Adenovirus RIDβ subunit contains a tyrosine residue that is critical for RID-mediated receptor internalization and inhibition of Fas- and TRAIL-induced apoptosis. J. Virol. 76, 11329-11342.
37. Lichtenstein, D.L., Doronin, K., Toth, K., Kuppuswamy, M., Wold, W.S., and Tollefson, A.E. (2004a). Adenovirus E3-6.7K protein is required in conjunction with the E3-RID protein complex for the internalization and degradation of TRAIL receptor 2. J. Virol. 78, 12297-12307.
38. Lichtenstein, D.L., Toth, K., Doronin, K., Tollefson, A.E., and Wold, W.S. (2004b). Functions and mechanisms of action of the adenovirus E3 proteins. Int. Rev. Immunol. 23, 75-111.
39. Louis, N., Fender, P., Barge, A., Kitts, P., and Chroboczek, J. (1994). Cell binding domain of adenovirus serotype 2 fiber. J. Virol. 68, 4104-4106.
40. Luo, X., Budihardjo, I., Zou, H., Slaughter, C., and Wang, X. (1998). Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94, 481-490.
41. Ma, H., Liu, Y., Liu, S., Kung, H.F., Sun, X., Zheng, D., and Xu, R. (2005). Recombinant adeno-associated virus-mediated TRAIL gene therapy suppresses liver metastatic tumors. Int. J. Cancer 116, 314-321.
42. Macfarlane, M., Harper, N., Snowden, R.T., Dyer, M.J., Barnett, G.A., Pringle, J.H., and Cohen, G.M. (2002). Mechanisms of resistance to TRAIL induced apoptosis in primary B cell chronic lymphocytic leukaemia. Oncogene 21, 6809-6818.
43. Martelli, A.M., Tazzari, P.L., Tabellini, G., Bortul, R., Billi, A.M., Manzoli, L., Ruggeri, A., Conte, R., and Cocco, L. (2003). A new selective AKT pharmacological inhibitor reduces resistance to chemotherapeutic drugs, TRAIL, all-trans-retinoic acid, and ionizing radiation of human leukemia cells. Leukemia 17, 1794-1805.
44. McGahon, A., Bissonnette, R., Schmitt, M., Cotter, K.M., Green, D.R., and Cotter, T.G. (1994). BCR-ABL maintains resistance of chronic myelogenous leukemia cells to apoptotic cell death. Blood 83, 1179-1187.
45. Mi, J., Li, Z.Y., Ni, S., Steinwaerder, D., and Lieber, A. (2001). Induced apoptosis supports spread of adenovirus vectors in tumors. Hum. Gene Ther. 12, 1343-1352.
46. Nagane, M., Huang, H.J., and Cavenee, W.K. (2001). The potential of TRAIL for cancer chemotherapy. Apoptosis 6, 191-197.
47. Ni, S., Bernt, K., Gaggar, A., Li, Z.Y., Kiem, H.P., and Lieber, A. (2005). Evaluation of biodistribution and safety of adenovirus vectors containing group B fibers after intravenous injection into baboons. Hum. Gene Ther. 16, 664-677.
48. Nimmanapalli, R., Porosnicu, M., Nguyen, D., Worthington, E., O'Bryan, E., Perkins, C., and Bhalla, K. (2001). Cotreatment with STI-571 enhances tumor necrosis factor α-related apoptosis-inducing ligand (TRAIL or apo-2L)-induced apoptosis of Bcr-Abl-positive human acute leukemia cells. Clin. Cancer Res. 7, 350-357.
49. Ogretmen, B., and Safa, A.R. (2000). Identification and characterization of the MDR1 promoter-enhancing factor 1 (MEF1) in the multidrug resistant HL60/VCR human acute myeloid leukemia cell line. Biochemistry 39, 194-204.
50. Ozoren, N., Kim, K., Burns, T.F., Dicker, D.T., Moscioni, A.D., and Eldeiry, W.S. (2000). The caspase 9 inhibitor Z-LEHD-FMK protects human liver cells while permitting death of cancer cells exposed to tumor necrosis factor related apoptosis-inducing ligand. Cancer Res. 60, 6259-6265.
51. Park, S.J., Wu, C.H., Choi, M.R., Najafi, F., Emami, A., and Safa, A.R. (2006). P-glycoprotein enhances TRAIL-triggered apoptosis in multidrug resistant cancer cells by interacting with the death receptor DR5. Biochem. Pharmacol. 72, 293-307.
52. Pitti, R.M., Marsters, S.A., Ruppert, S., Donahue, C.J., Moore, A., and Ashkenazi, A. (1996). Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J. Biol. Chem. 271, 12687-12690.
53. Poulaki, V., Mitsiades, C.S., Kotoula, V., Tseleni-Balafouta, S., Ashkenazi, A., Koutras, D.A., and Mitsiades, N. (2002). Regulation of Apo2L/tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis in thyroid carcinoma cells. Am. J. Pathol. 161, 643-654.
54. Ruigrok, R.W., Barge, A., Albiges-Rizo, C., and Dayan, S. (1990). Structure of adenovirus fibre. II. Morphology of single fibres. J. Mol. Biol. 215, 589-596.
55. Salvesen, G.S., and Dixit, V.M. (1997). Caspases: Intracellular signaling by proteolysis. Cell 91, 443-446.
56. Salvesen, G.S., and Dixit, V.M. (1999). Caspase activation: The induced-proximity model. Proc. Natl. Acad. Sci. U.S.A. 96, 10964-10967.
57. Segerman, A., Arnberg, N., Erikson, A., Lindman, K., and Wadell, G. (2003). There are two different species B adenovirus receptors: sBAR, common to species B1 and B2 adenoviruses, and sB2AR, exclusively used by species B2 adenoviruses. J. Virol. 77, 1157-1162.
58. Seshidhar Reddy, P., Ganesh, S., Limbach, M.P., Brann, T., Pinkstaff, A., Kaloss, M., Kaleko, M., and Connelly, S. (2003). Development of adenovirus serotype 35 as a gene transfer vector. Virology 311, 384-393.
59. + cells by a retargeted adenovirus vector. J. Virol. 74, 2567-2583.
60. Shiiki, K., Yoshikawa, H., Kinoshita, H., Takeda, M., Ueno, A., Nakajima, Y., and Tasaka, K. (2000). Potential mechanisms of resistance to TRAIL/Apo2L-induced apoptosis in human promyelocytic leukemia HL-60 cells during granulocytic differentiation. Cell Death Differ. 7, 939-946.
61. Srinivasula, S.M., Ahmad, M., Guo, Y., Zhan, Y., Lazebnik, Y., Fernandes-Alnemri, T., and Alnemri, E.S. (1999). Identification of an endogenous dominant-negative short isoform of caspase-9 that can regulate apoptosis. Cancer Res. 59, 999-1002.
62. Suliman, A., Lam, A., Datta, R., and Srivastava, R.K. (2001). Intracellular mechanisms of TRAIL: Apoptosis through mitochondrial-dependent and -independent pathways. Oncogene 20, 2122-2133.
63. Tollefson, A.E., Toth, K., Doronin, K., Kuppuswamy, M., Doronina, O.A., Lichtenstein, D.L., Hermiston, T.W., Smith, C.A., and Wold, W.S. (2001). Inhibition of TRAIL-induced apoptosis and forced internalization of TRAIL receptor 1 by adenovirus proteins. J. Virol. 75, 8875-8887.
64. Trauzold, A., Siegmund, D., Schniewind, B., Sipos, B., Egberts, J., Zorenkov, D., Emme, D., Roder, C., Kalthoff, H., and Wajant, H. (2006). TRAIL promotes metastasis of human pancreatic ductal adenocarcinoma. Oncogene 25, 7434-7439.
65. van Oostrum, J., and Burnett, R.M. (1985). Molecular composition of the adenovirus type 2 virion. J. Virol. 56, 439-448.
66. Wiley, S.R., Schooley, K., Smolak, P.J., Din, W.S., Huang, C.P., Nicholl, J.K., Sutherland, G.R., Smith, T.D., Rauch, C., Smith, C.A., and Goodwin, R.G. (1995). Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 3, 673-682.
67. Yotnda, P., Zompeta, C., Heslop, H.E., Andreeff, M., Brenner, M.K., and Marini, F. (2004). Comparison of the efficiency of transduction of leukemic cells by fiber-modified adenoviruses. Hum. Gene Ther. 15, 1229-1242.
68. L expression is necessary and sufficient to maintain resistance to tumor necrosis factor-related apoptosis-inducing ligand mediated apoptosis in prostate cancer. Cancer Res. 64, 7086-7091.
69. Zhang, X.D., Franco, A., Myers, K., Gray, C., Nguyen, T., and Hersey, P. (1999). Relation of TNF-related apoptosis-inducing ligand (TRAIL) receptor and FLICE-inhibitory protein expression to TRAIL-induced apoptosis of melanoma. Cancer Res. 59, 2747-2753.
70. Zou, H., Li, Y., Liu, X., and Wang, X. (1999). An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem. 274, 11549-11556.
71. Zuzak, T.J., Steinhoff, D.F., Sutton, L.N., Phillips, P.C., Eggert, A., and Grotzer, M.A. (2002). Loss of caspase-8 mRNA expression is common in childhood primitive neuroectodermal brain tumour/medulloblastoma. Eur. J. Cancer 38, 83-91