Potent antitumor activity of oncolytic adenovirus expressing Beclin-1 via induction of autophagic cell death in leukemia

Oncotarget

Volumn 4, Issue 6, 2013, Pages 860-874

  Tong, Yin ^a   You, Liangshun ^a   Liu, Hui ^a   Li, Lu ^a   Meng, Haitao ^a   Qian, Qijun ^b   Qian, Wenbin ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Autophagic cell death; Autophagy; Beclin 1; Leukemia; Oncolytic adenovirus; UVRAG

Indexed keywords

ADENOVIRUS VECTOR; AUTOPHAGY PROTEIN 5; BECLIN 1; COMPLEMENTARY DNA; IMATINIB; ONCOLYTIC ADENOVIRUS; RNA;

ACUTE GRANULOCYTIC LEUKEMIA; ADULT; AGED; ANIMAL EXPERIMENT; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL DEATH; CELL KILLING; CHRONIC MYELOID LEUKEMIA; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; FEMALE; GENE EXPRESSION; HUMAN; IN VITRO STUDY; LEUKEMIA CELL; MALE; MOUSE; NONHUMAN; ONCOLYTIC VIROTHERAPY; PROTEIN EXPRESSION; RNA INTERFERENCE; TUMOR CELL;

ADENOVIRIDAE; ADULT; AGED; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CELL LINE, TUMOR; FEMALE; HUMANS; K562 CELLS; LEUKEMIA; MALE; MEMBRANE PROTEINS; MICE; MIDDLE AGED; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; RANDOM ALLOCATION; TRANSFECTION; XENOGRAFT MODEL ANTITUMOR ASSAYS; YOUNG ADULT;

EID: 84880786463     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1018     Document Type: Article

References (59)

1. Eager RM, Nemunaitis J. Clinical development directions in oncolytic viral therapy. Cancer Gene Ther. 2011;18(5):305-317.
2. Zhang Q, Chen G, Peng L, Wang X, Yang Y, Liu C, Shi W, Su C, Wu H, Liu X, Wu M, Qian Q. Increased safety with preserved antitumoral efficacy on hepatocellular carcinoma with dual-regulated oncolytic adenovirus. Clin Cancer Res. 2006;12(21):6523-6531.
3. Jin H, Lv S, Yang J, Wang X, Hu H, Su C, Zhou C, Li J, Huang Y, Li L, Liu X, Wu M, Qian Q. Use of microRNA Let-7 to control the replication specificity of oncolytic adenovirus in hepatocellular carcinoma cells. PLoS One. 2011;6(7):e21307.
4. Vasey PA, Shulman LN, Campos S, Davis J, Gore M, Johnston S, Kirn DH, O'Neill V, Siddiqui N, Seiden MV, Kaye SB. Phase I trial of intraperitoneal injection of the E1B-55-kd-gene-deleted adenovirus ONYX-015 (dl1520) given on days 1 through 5 every 3 weeks in patients with recurrent/refractory epithelial ovarian cancer. J Clin Oncol. 2002;20(6):1562-1569.
5. Kimball KJ, Preuss MA, Barnes MN, Wang M, Siegal GP, Wan W, Kuo H, Saddekni S, Stockard CR, Grizzle WE, Harris RD, Aurigemma R, Curiel DT, Alvarez RD. A phase I study of a tropism-modified conditionally replicative adenovirus for recurrent malignant gynecologic diseases. Clin Cancer Res. 2010;16(21):5277-5287.
6. Short JJ, Curiel DT. Oncolytic adenoviruses targeted to cancer stem cells. Mol Cancer Ther. 2009;8(8):2096-2102.
7. Rivera AA, Davydova J, Schierer S, Wang M, Krasnykh V, Yamamoto M, Curiel DT, Nettelbeck DM. Combining high selectivity of replication with fiber chimerism for effective adenoviral oncolysis of CAR-negative melanoma cells. Gene Ther. 2004;11(23):1694-1702.
8. Jin J, Liu H, Yang C, Li G, Liu X, Qian Q, Qian W. Effective gene-viral therapy of leukemia by a new fiber chimeric oncolytic adenovirus expressing TRAIL: in vitro and in vivo evaluation. Mol Cancer Ther. 2009;8(5):1387-1397.
9. Ranki T, Hemminki A.Serotype chimeric human adenoviruses for cancer gene therapy. Viruses. 2010;2(10):2196-2212.
10. Koski A, Kangasniemi L, Escutenaire S, Pesonen S, CerulloV, Diaconu I, Nokisalmi P, Raki M, Rajecki M, Guse K, Ranki T, Oksanen M, Holm SL, Haavisto E, Karioja-Kallio A, Laasonen L, et al. Treatment of cancer patients with a serotype 5/3 chimeric oncolytic adenovirus expressing GMCSF. Mol Ther. 2010;18(10):1874-1884.
11. Pesonen S, Nokisalmi P, Escutenaire S, Särkioja M, Raki M, Cerullo V, Kangasniemi L, Laasonen L, Ribacka C, Guse K, Haavisto E, Oksanen M, Rajecki M, Helminen A, Ristimäki A, Karioja-Kallio A, et al. Prolonged systemic circulation of chimeric oncolytic adenovirus Ad5/3-Cox2L-D24 in patients with metastatic and refractory solid tumors. Gene Ther. 2010;17(7):892-904.
12. Cripe TP, Wang PY, Marcato P, Mahller YY, Lee PW. Targeting cancer-initiating cells with oncolytic viruses. Mol Ther. 2009;17(10):1677-1682.
13. Eriksson M, Guse K, Bauerschmitz G, Virkkunen P, Tarkkanen M, Tanner M, Hakkarainen T, Kanerva A, Desmond RA, Pesonen S, Hemminki A. Oncolytic adenoviruses kill breast cancer initiating CD44+CD24-/low cells. Mol Ther. 2007;15(12):2088-2093.
14. Hermiston T. Gene delivery from replication-selective viruses: arming guided missiles in the war against cancer. J Clin Invest. 2000;105(9):1169-1172.
15. Liu XY, Qiu SB, Zou WG, Pei ZF, Gu JF, Luo CX, Ruan HM, Chen Y, Qi YP, Qian C. Effective gene-virotherapy for complete eradication of tumor mediated by the combination of hTRAIL (TNFSF10) and plasminogen k5. Mol Ther. 2005;11(4):531-541.
16. Dong F, Wang L, Davis JJ, Hu W, Zhang L, Guo W, Teraishi F, Ji L, Fang B. Eliminating established tumor in nu/nu nude mice by a tumor necrosis factor-alpha-related apoptosis-inducing ligand-armed oncolytic adenovirus. Clin Cancer Res. 2006;12(17):5224-5230.
17. Cody JJ, Douglas JT. Armed replicating adenoviruses for cancer virotherapy. Cancer Gene Ther. 2009;16(6):473-488.
18. Wong HH, Lemoine NR, Wang Y. Viruses. Oncolytic Viruses for Cancer Therapy: Overcoming the Obstacles. Viruses. 2010;2(1):78-106.
19. He X, Liu J, Yang C, Su C, Zhou C, Zhang Q, Li L, Wu H, Liu X, Wu M, Qian Q.5/35 fiber-modified conditionally replicative adenovirus armed with p53 shows increased tumor-suppressing capacity to breast cancer cells. Hum Gene Ther. 2011;22(3):283-292.
20. Yang C, Tong Y, Ni W, Liu J, Xu W, Li L, Liu X, Meng H, Qian W. Inhibition of autophagy induced by overexpression of mda-7/interleukin-24 strongly augments the antileukemia activity in vitro and in vivo.Cancer Gene Ther. 2010;17(2):109-119.
21. Mashima T, Tsuruo T.Defects of the apoptotic pathway as therapeutic target against cancer. Drug Resist Updat. 2005;8(6):339-343.
22. Chen N, Karantza V.Autophagy as a therapeutic target in cancer. Cancer Biol Ther. 2011;11(2):157-168.
23. Chen Y, McMillan-Ward E, Kong J, Israels SJ, Gibson SB. Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Cell Death Differ. 2008;15(1):171-182.
24. Høyer-Hansen M, Bastholm L, Mathiasen IS, Elling F, Jäättelä M. Vitamin D analog EB1089 triggers dramatic lysosomal changes and Beclin 1-mediated autophagic cell death. Cell Death Differ.2005;12(10):1297-1309.
25. Qian W, Liu J, Jin J, Ni W, Xu W. Arsenic trioxide induces not only apoptosis but also autophagic cell death in leukemia cell lines via up-regulation of Beclin-1. Leuk Res. 2007;31(3):329-339.
26. Carew JS, Nawrocki ST, Kahue CN, Zhang H, Yang C, Chung L, Houghton JA, Huang P, Giles FJ, Cleveland JL. Targeting autophagy augments the anticancer activity of the histone deacetylase inhibitor SAHA to overcome Bcr-Ablmediated drug resistance. Blood. 2007;110(1):313-322.
27. Liang XH, Yu J, Brown K, Levine B. Beclin 1 contains a leucine-rich nuclear export signal that is required for its autophagy and tumor suppressor function. Cancer Res. 2001;61(8):3443-3449.
28. Perrotta I, Carito V, Russo E, Tripepi S, Aquila S, Donato G. Macrophage autophagy and oxidative stress: an ultrastructural and immunoelectron microscopical study. Oxid Med Cell Longev. 2011;2011:282739.
29. Liang C, Feng P, Ku B, Dotan I, Canaani D, Oh BH, Jung JU. Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat Cell Biol. 2006;8(7):688-699.
30. Laane E, Tamm KP, Buentke E, Ito K, Kharaziha P, Oscarsson J, Corcoran M, Björklund AC, Hultenby K, Lundin J, Heyman M, Söderhäll S, Mazur J, Porwit A, Pandolfi PP, Zhivotovsky B, et al. Cell death induced by dexamethasone in lymphoid leukemia is mediated through initiation of autophagy. Cell Death Differ. 2009;16(7):1018-1029.
31. Goussetis DJ, Altman JK, Glaser H, McNeer JL, Tallman MS, Platanias LC.Autophagy is a critical mechanism for the induction of the antileukemic effects of arsenic trioxide. J Biol Chem. 2010;285(39):29989-29997.
32. Heidari N, Hicks MA, Harada H. GX15-070 (obatoclax) overcomes glucocorticoid resistance in acute lymphoblastic leukemia through induction of apoptosis and autophagy. Cell Death Dis. 2010;1:e76.
33. Bonapace L, Bornhauser BC, Schmitz M, Cario G, Ziegler U, Niggli FK, Schäfer BW, Schrappe M, Stanulla M, Bourquin JP. Induction of autophagy-dependent necroptosis is required for childhood acute lymphoblastic leukemia cells to overcome glucocorticoid resistance. J Clin Invest. 2010;120(4):1310-1323.
34. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B. Induction of autophagy and inhibition of tumorigenesis by beclin-1. Nature. 1999;402(6762):672-676.
35. Kihara A, Kabeya Y, Ohsumi Y, Yoshimori T. Beclinphosphatidylinositol 3-kinase complex functions at the trans-Golgi network.EMBO Rep. 2001;2(4):330-335.
36. He C, Levine B. The beclin 1 interactome. Curr Opin Cell Biol. 2010 Apr;22(2):140-9.
37. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A, Rosen J, Eskelinen EL, Mizushima N, Ohsumi Y, Cattoretti G, Levine B. Promotion of tumorigenesis by heterozygous disruption of the beclin-1 autophagy gene. J Clin Invest. 2003;112(12):1809-1820.
38. Yue Z, Jin S, Yang C, Levine AJ, Heintz N. Beclin-1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci U S A. 2003;100(25):15077-15082.
39. Dalby KN, Tekedereli I, Lopez-Berestein G, Ozpolat B. Targeting the prodeath and prosurvival functions of autophagy as novel therapeutic strategies in cancer. Autophagy. 2010;6(3):322-329.
40. Ding ZB, Shi YH, Zhou J, Qiu SJ, Xu Y, Dai Z, Shi GM, Wang XY, Ke AW, Wu B, Fan J. Association of autophagy defect with a malignant phenotype and poor prognosis of hepatocellular carcinoma. Cancer Res. 2008;68(22):9167-9175.
41. Zhou WH, Tang F, Xu J, Wu X, Yang SB, Feng ZY, Ding YG, Wan XB, Guan Z, Li HG, Lin DJ, Shao CK, Liu Q. Low expression of Beclin 1, associated with high BclxL, predicts a malignant phenotype and poor prognosis of gastric cancer. Autophagy. 2012; 8(3):389-400.
42. Huang JJ, Zhu YJ, Lin TY, Jiang WQ, Huang HQ, Li ZM. Beclin 1 expression predicts favorable clinical outcome in patients with diffuse large B-cell lymphoma treated with R-CHOP. Hum Pathol. 2011;42(10):1459-1466.
43. Liang LZ, Ma B, Liang YJ, Liu HC, Zheng GS, Zhang TH, Chu M, Xu PP, Su YX, Liao GQ. High expression of the autophagy gene Beclin-1 is associated with favorable prognosis for salivary gland adenoid cystic carcinoma. J Oral Pathol Med. 2012;41(8):621-629.
44. Elgendy M, Sheridan C, Brumatti G, Martin SJ. Oncogenic Ras-induced expression of Noxa and Beclin-1 promotes autophagic cell death and limits clonogenic survival. Mol Cell 2011;42(1):23-35.
45. Mancias JD, Kimmelman AC. Targeting autophagy addiction in cancer. Oncotarget. 2011;2(12):1302-1306.
46. Chiarini F, Lonetti A, Teti G, Orsini E, Bressanin D, Cappellini A, Ricci F, Tazzari PL, Ognibene A, Falconi M, Pagliaro P, Iacobucci I, Martinelli G, Amadori S, McCubrey JA, Martelli AM. A combination of temsirolimus, an allosteric mTOR inhibitor, with clofarabine as a new therapeutic option for patients with acute myeloid leukemia. Oncotarget. 2012;3(12):1615-1628.
47. Criollo A, Chereau F, Malik SA, Niso-Santano M, Mariño G, Galluzzi L, Maiuri MC, Baud V, Kroemer G. Autophagy is required for the activation of NF?B. Cell Cycle. 2012;11(1):194-199.
48. Boehrer S, Galluzzi L, Lainey E, Bouteloup C, Tailler M, Harper F, Pierron G, Adés L, Thépot S, Sébert M, Gardin C, de Botton S, Fenaux P, Kroemer G. Erlotinib antagonizes constitutive activation of SRC family kinases and mTOR in acute myeloid leukemia. Cell Cycle. 2011;10(18):3168-3175.
49. Cufí S, Vazquez-Martin A, Oliveras-Ferraros C, Corominas-Faja B, Urruticoechea A, Martin-Castillo B, Menendez JA. Autophagy-related gene 12 (ATG12) is a novel determinant of primary resistance to HER2-targeted therapies: utility of transcriptome analysis of the autophagy interactome to guide breast cancer treatment. Oncotarget. 2012;3(12):1600-1614.
50. Akar U, Chaves-Reyez A, Barria M, Tari A, Sanguino A, Kondo Y, Kondo S, Arun B, Lopez-Berestein G, Ozpolat B. Silencing Bcl-2 expression by small interfering RNA induces autophagic cell death in MCF-7 breast cancer cells. Autophagy. 2008;4(5):669-679.
51. Crazzolara R, Cisterne A, Thien M, Hewson J, Baraz R, Bradstock KF, Bendall LJ. Potentiating effects of RAD001 (Everolimus) on vincristine therapy in childhood acute lymphoblastic leukemia. Blood. 2009;113(14):3297-3306.
52. Guo W, Zhu H, Zhang L, Davis J, Teraishi F, Roth JA, Stephens C, Fueyo J, Jiang H, Conrad C, Fang B. Combination effect of oncolytic adenovirotherapy and TRAIL gene therapy in syngeneic murine breast cancer models. Cancer Gene Ther. 2006;13(1):82-90.
53. Bischoff JR, Kirn DH, Williams A, Heise C, Horn S, Muna M, Ng L, Nye JA, Sampson-Johannes A, Fattaey A, McCormick F. An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science 1996; 274(5286):373-376.
54. Dix BR, Edwards SJ, Braithwaite AW. Does the antitumor adenovirus ONYX-015/dl1520 selectively target cells defective in the p53 pathway? J Virol 2001; 75 (12):5443-5447.
55. Thaci B, Ulasov IV, Wainwright DA, Lesniak MS. The challenge for gene therapy: innate immune response to adenoviruses. Oncotarget. 2011;2(3):113-121
56. Donnelly O, Vile R, Pandha H, Harrington K, Melcher A. The hitchhiker's guide to virotherapy. Oncotarget. 2012;3(8):735-736.
57. Kishimoto H, Aki R, Urata Y, Bouvet M, Momiyama M, Tanaka N, Fujiwara T, Hoffman RM. Tumor-selective, adenoviral-mediated GFP genetic labeling of human cancer in the live mouse reports future recurrence after resection. Cell Cycle. 2011;10(16):2737-2741.
58. Lin WH, Yeh SH, Yang WJ, Yeh KH, Fujiwara T, Nii A, Chang SS, Chen PJ. Telomerase-specific oncolytic adenoviral therapy for orthotopic hepatocellular carcinoma in HBx transgenic mice. Int J Cancer. 2013;132(6):1451-1462.Z. Msi-1 is a predictor of survival and a novel therapeutic target in colon cancer. Ann Surg Oncol. 2011; 18(7):2074-2083.
59. Msi-1 is. a predictor of survival and a novel therapeutic target in colon cancer. Ann Surg Oncol. 2011; 18(7):2074-2083.