Combination of autophagy inducer rapamycin and oncolytic adenovirus improves antitumor effect in cancer cells

Virology Journal

Volumn 10, Issue , 2013, Pages

  Cheng, Pei Hsin ^a   Lian, Serena ^a   Zhao, Robin ^a   Rao, Xiao Mei ^a   McMasters, Kelly M ^a   Zhou, Heshan Sam ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

Autophagy; Cyclin E; Oncolytic adenovirus; Rapamycin; Replication

Indexed keywords

ONCOLYTIC ADENOVIRUS; RAPAMYCIN;

ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOPHAGY; CANCER CELL; CELL VIABILITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFECT; HUMAN; HUMAN CELL;

ADENOVIRIDAE;

ADENOVIRIDAE; AUTOPHAGY; CELL LINE; CELL SURVIVAL; HUMANS; ONCOLYTIC VIRUSES; SIROLIMUS; VIRAL LOAD; VIRUS REPLICATION;

EID: 84884365359     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/1743-422X-10-293     Document Type: Article

References (81)

1. Clinical trials with oncolytic adenovirus in China. Yu W, Fang H, Curr Cancer Drug Targets 2007 7 141 148 10.2174/156800907780058817 17346105 (Pubitemid 46348628)
2. Clinical development directions in oncolytic viral therapy. Eager RM, Nemunaitis J, Cancer Gene Ther 2011 18 305 317 10.1038/cgt.2011.7 21436867
3. A new generation of serotype chimeric infectivity-enhanced conditionally replicative adenovirals: the safety profile of ad5/3-Delta24 in advance of a phase I clinical trial in ovarian cancer patients. Kim KH, Ryan MJ, Estep JE, Miniard BM, Rudge TL, Peggins JO, Broadt TL, Wang M, Preuss MA, Siegal GP, et al. Hum Gene Ther 2011 22 821 828 10.1089/hum.2010.180 21171861
4. A phase I study of telomerase-specific replication competent oncolytic adenovirus (telomelysin) for various solid tumors. Nemunaitis J, Tong AW, Nemunaitis M, Senzer N, Phadke AP, Bedell C, Adams N, Zhang YA, Maples PB, Chen S, et al. Mol Ther 2010 18 429 434 10.1038/mt.2009.262 19935775
5. A phase I study of a tropism-modified conditionally replicative adenovirus for recurrent malignant gynecologic diseases. Kimball KJ, Preuss MA, Barnes MN, Wang M, Siegal GP, Wan W, Kuo H, Saddekni S, Stockard CR, Grizzle WE, et al. Clin Cancer Res 2010 16 5277 5287 10.1158/1078-0432.CCR-10-0791 20978148
6. Oncolytic viral therapy of malignant glioma. Parker JN, Bauer DF, Cody JJ, Markert JM, Neurotherapeutics 2009 6 558 569 10.1016/j.nurt.2009.04.011 19560745
7. Chapter three-Syrian hamster as an animal model to study oncolytic adenoviruses and to evaluate the efficacy of antiviral compounds. Wold WS, Toth K, Adv Cancer Res 2012 115 69 92 23021242
8. Effect of intratracheal adenoviral vector administration on lung development in newborn rats. Waszak P, Franco-Montoya ML, Jacob MP, Deprez I, Levame M, Lafuma C, Harf A, Delacourt C, Hum Gene Ther 2002 13 1873 1885 10.1089/104303402760372963 12396619 (Pubitemid 35292682)
9. Intelligent design: combination therapy with oncolytic viruses. Ottolino-Perry K, Diallo JS, Lichty BD, Bell JC, McCart JA, Mol Ther 2010 18 251 263 10.1038/mt.2009.283 20029399
10. Adenoviruses induce autophagy to promote virus replication and oncolysis. Rodriguez-Rocha H, Gomez-Gutierrez JG, Garcia-Garcia A, Rao XM, Chen L, McMasters KM, Zhou HS, Virology 2011 416 9 15 10.1016/j.virol.2011.04.017 21575980
11. The role of autophagy in cancer development and response to therapy. Kondo Y, Kanzawa T, Sawaya R, Kondo S, Nat Rev Cancer 2005 5 726 734 10.1038/nrc1692 16148885 (Pubitemid 41486365)
12. Purification and characterization of autophagosomes from rat hepatocytes. Stromhaug PE, Berg TO, Fengsrud M, Seglen PO, Biochem J 1998 335 Pt 2 217 224 9761717 (Pubitemid 28491054)
13. Methods for detecting autophagy and determining autophagy-induced cell death. Chen Y, Azad MB, Gibson SB, Can J Physiol Pharmacol 2010 88 285 295 10.1139/Y10-010 20393593
14. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T, EMBO J 2000 19 5720 5728 10.1093/emboj/19.21.5720 11060023
15. Methods for monitoring autophagy. Mizushima N, Int J Biochem Cell Biol 2004 36 2491 2502 10.1016/j.biocel.2004.02.005 15325587 (Pubitemid 39119761)
16. How to interpret LC3 immunoblotting. Mizushima N, Yoshimori T, Autophagy 2007 3 542 545 17611390 (Pubitemid 350060049)
17. When autophagy meets viruses: a double-edged sword with functions in defense and offense. Kim HJ, Lee S, Jung JU, Semin Immunopathol 2010 32 323 341 10.1007/s00281-010-0226-8 20865416
18. Autophagy: assays and artifacts. Barth S, Glick D, Macleod KF, J Pathol 2010 221 117 124 10.1002/path.2694 20225337
19. Growing roles for the mTOR pathway. Sarbassov DD, Ali SM, Sabatini DM, Curr Opin Cell Biol 2005 17 596 603 10.1016/j.ceb.2005.09.009 16226444 (Pubitemid 41540408)
20. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Sarbassov DD, Ali SM, Sengupta S, Sheen JH, Hsu PP, Bagley AF, Markhard AL, Sabatini DM, Mol Cell 2006 22 159 168 10.1016/j.molcel.2006.03.029 16603397
21. Synergistic augmentation of rapamycin-induced autophagy in malignant glioma cells by phosphatidylinositol 3-kinase/protein kinase B inhibitors. Takeuchi H, Kondo Y, Fujiwara K, Kanzawa T, Aoki H, Mills GB, Kondo S, Cancer Res 2005 65 3336 3346 15833867 (Pubitemid 40524618)
22. Adenovirus and cell cycle control. Ben-Israel H, Kleinberger T, Front Biosci 2002 7 1369 1395 10.2741/ben 11991831
23. Oncolysis and suppression of tumor growth by a GFP-expressing oncolytic adenovirus controlled by an hTERT and CMV hybrid promoter. Davis JJ, Wang L, Dong F, Zhang L, Guo W, Teraishi F, Xu K, Ji L, Fang B, Cancer Gene Ther 2006 13 720 723 10.1038/sj.cgt.7700944 16485010 (Pubitemid 44264475)
24. A strict-late viral promoter is a strong tumor-specific promoter in the context of an oncolytic herpes simplex virus. Fu X, Meng F, Tao L, Jin A, Zhang X, Gene Ther 2003 10 1458 1464 10.1038/sj.gt.3302029 12900760 (Pubitemid 36987139)
25. Gene expression profiles of normal human lung cells affected by adenoviral E1B. Rao XM, Zheng X, Waigel S, Zacharias W, McMasters KM, Zhou HS, Virology 2006 350 418 428 10.1016/j.virol.2006.02.009 16542696 (Pubitemid 43928107)
26. Oncolytic (replication-competent) adenoviruses as anticancer agents. Toth K, Dhar D, Wold WS, Expert Opin Biol Ther 2010 10 353 368 10.1517/ 14712590903559822 20132057
27. Selectivity of a replication-competent adenovirus for human breast carcinoma cells expressing the MUC1 antigen. Kurihara T, Brough DE, Kovesdi I, Kufe DW, J Clin Invest 2000 106 763 771 10.1172/JCI9180 10995787
28. Distinct roles for cyclins E and A during DNA replication complex assembly and activation. Coverley D, Laman H, Laskey RA, Nat Cell Biol 2002 4 523 528 10.1038/ncb813 12080347 (Pubitemid 34752439)
29. Cyclin E uses Cdc6 as a chromatin-associated receptor required for DNA replication. Furstenthal L, Kaiser BK, Swanson C, Jackson PK, J Cell Biol 2001 152 1267 1278 10.1083/jcb.152.6.1267 11257126 (Pubitemid 34280183)
30. Cyclin E in human cancers. Donnellan R, Chetty R, FASEB J 1999 13 773 780 10224221 (Pubitemid 29220690)
31. A mouse model for cyclin E-dependent genetic instability and tumorigenesis. Loeb KR, Kostner H, Firpo E, Norwood T, DTsuchiya K, Clurman BE, Roberts JM, Cancer Cell 2005 8 35 47 10.1016/j.ccr.2005.06.010 16023597 (Pubitemid 40991813)
32. Cyclin E transgenic mice: discovery tools for lung cancer biology, therapy, and prevention. Freemantle SJ, Dmitrovsky E, Cancer Prev Res (Phila) 2010 3 1513 1518 10.1158/1940-6207.CAPR-10-0297
33. Adenovirus E1B55K region is required to enhance cyclin E expression for efficient viral DNA replication. Zheng X, Rao XM, Gomez-Gutierrez JG, Hao H, McMasters KM, Zhou HS, J Virol 2008 82 3415 3427 10.1128/JVI.01708-07 18234796 (Pubitemid 351429918)
34. Selective replication of E1B55K-deleted adenoviruses depends on enhanced E1A expression in cancer cells. Zheng X, Rao XM, Snodgrass CL, McMasters KM, Zhou HS, Cancer Gene Ther 2006 13 572 583 10.1038/sj.cgt.7700923 16341141
35. Enhanced cancer cell killing by truncated E2F-1 used in combination with oncolytic adenovirus. Gomez-Gutierrez JG, Rao XM, Zhou HS, McMasters KM, Virology 2012 433 538 547 10.1016/j.virol.2012.09.003 23021422
36. The Limited in Vitro Lifetime of Human Diploid Cell Strains. Hayflick L, Exp Cell Res 1965 37 614 636 10.1016/0014-4827(65)90211-9 14315085
37. Parabens enable suspension growth of MCF-10A immortalized, non-transformed human breast epithelial cells. Khanna S, Darbre PD, J Appl Toxicol 2013 33 378 382 10.1002/jat.2753 22744862
38. Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Soule HD, Maloney TM, Wolman SR, Peterson WD Jr, Brenz R, McGrath CM, Russo J, Pauley RJ, Jones RF, Brooks SC, Cancer Res 1990 50 6075 6086 1975513 (Pubitemid 20331424)
39. Molecular basis for viral selective replication in cancer cells: activation of CDK2 by adenovirus-induced cyclin E. Cheng PH, Rao XM, McMasters KM, Zhou HS, PLoS One 2013 8 57340 10.1371/journal.pone.0057340 23437375
40. Regulation of cyclin E transcription by E2Fs and retinoblastoma protein. Geng Y, Eaton EN, Picon M, Roberts JM, Lundberg AS, Gifford A, Sardet C, Weinberg RA, Oncogene 1996 12 1173 1180 8649818 (Pubitemid 26127247)
41. A combined assay of cell viability and in vitro cytotoxicity with a highly water-soluble tetrazolium salt, neutral red and crystal violet. Ishiyama M, Tominaga H, Shiga M, Sasamoto K, Ohkura Y, Ueno K, Biol Pharm Bull 1996 19 1518 1520 10.1248/bpb.19.1518 8951178 (Pubitemid 26403266)
42. A hypoxia- and {alpha}-fetoprotein-dependent oncolytic adenovirus exhibits specific killing of hepatocellular carcinomas. Kwon OJ, Kim PH, Huyn S, Wu L, Kim M, Yun CO, Clin Cancer Res 2010 16 6071 6082 10.1158/1078-0432.CCR- 10-0664 21169258
43. Synergistic, additive, and antagonistic effects of food mixtures on total antioxidant capacities. Wang S, Meckling KA, Marcone MF, Kakuda Y, Tsao R, J Agric Food Chem 2011 59 960 968 10.1021/jf1040977 21222468
44. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Chou TC, Pharmacol Rev 2006 58 621 681 10.1124/pr.58.3.10 16968952 (Pubitemid 44403686)
45. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Chou TC, Talalay P, Adv Enzyme Regul 1984 22 27 55 6382953
46. Exploitable mechanisms in combined radiotherapy-chemotherapy: the concept of additivity. Steel GG, Peckham MJ, Int J Radiat Oncol Biol Phys 1979 5 85 91 422420 (Pubitemid 9120186)
47. Evaluation of the in vitro anti-HBV activity of clevudine in combination with other nucleoside/nucleotide inhibitors. Niu C, Bao H, Tolstykh T, Micolochick Steuer HM, Murakami E, Korba B, Furman PA, Antivir Ther 2010 15 401 412 10.3851/IMP1541 20516559
48. Optimization of the helper-dependent adenovirus system for production and potency in vivo. Sandig V, Youil R, Bett AJ, Franlin LL, Oshima M, Maione D, Wang F, Metzker ML, Savino R, Caskey CT, Proc Natl Acad Sci U S A 2000 97 1002 1007 10.1073/pnas.97.3.1002 10655474 (Pubitemid 30080802)
49. Adenovirus with insertion-mutated E1A selectively propagates in liver cancer cells and destroys tumors in vivo. Zhao T, Rao XM, Xie X, Li L, Thompson TC, McMasters KM, Zhou HS, Cancer Res 2003 63 3073 3078 12810631 (Pubitemid 36735855)
50. Tp53-gene transfer induces hypersensitivity to low doses of X-rays in glioblastoma cells: a strategy to convert a radio-resistant phenotype into a radiosensitive one. D'Avenia P, Porrello A, Berardo M, Angelo MD, Soddu S, Arcangeli G, Sacchi A, D'Orazi G, Cancer Lett 2006 231 102 112 10.1016/j.canlet.2005.01.033 16356835 (Pubitemid 41779458)
51. Effect of sirolimus on urinary bladder cancer T24 cell line. Pinto-Leite R, Botelho P, Ribeiro E, Oliveira PA, Santos L, J Exp Clin Cancer Res 2009 28 3 10.1186/1756-9966-28-3 19128503
52. Combination therapy with conditionally replicating adenovirus and replication defective adenovirus. Lee CT, Park KH, Yanagisawa K, Adachi Y, Ohm JE, Nadaf S, Dikov MM, Curiel DT, Carbone DP, Cancer Res 2004 64 6660 6665 10.1158/0008-5472.CAN-04-1200 15374981 (Pubitemid 39297927)
53. In vivo imaging of adenovirus transduction and enhanced therapeutic efficacy of combination therapy with conditionally replicating adenovirus and adenovirus-p27. Lee CT, Lee YJ, Kwon SY, Lee J, Kim KI, Park KH, Kang JH, Yoo CG, Kim YW, Han SK, et al. Cancer Res 2006 66 372 377 10.1158/0008-5472.CAN-05- 1515 16397251 (Pubitemid 43166044)
54. Monoclonal antibodies specific for adenovirus early region 1A proteins: extensive heterogeneity in early region 1A products. Harlow E, Franza BR Jr, Schley C, J Virol 1985 55 533 546 3894685 (Pubitemid 16249658)
55. Generalized equations for the analysis of inhibitions of Michaelis-Menten and higher-order kinetic systems with two or more mutually exclusive and nonexclusive inhibitors. Chou TC, Talalay P, Eur J Biochem 1981 115 207 216 7227366
56. Oncolytic viruses in cancer therapy. Vaha-Koskela MJ, Heikkila JE, Hinkkanen AE, Cancer Lett 2007 254 178 216 10.1016/j.canlet.2007.02.002 17383089 (Pubitemid 47126688)
57. Clinical research results with dl1520 (Onyx-015), a replication-selective adenovirus for the treatment of cancer: what have we learned? Kirn D, Gene Ther 2001 8 89 98 10.1038/sj.gt.3301377 11313778 (Pubitemid 32162422)
58. Current issues and future directions of oncolytic adenoviruses. Yamamoto M, Curiel DT, Mol Ther 2010 18 243 250 10.1038/mt.2009.266 19935777
59. Host cell autophagy modulates early stages of adenovirus infections in airway epithelial cells. Zeng X, Carlin CR, J Virol 2013 87 2307 2319 10.1128/JVI.02014-12 23236070
60. Autophagy in the regulation of pathogen replication and adaptive immunity. Randow F, Munz C, Trends Immunol 2012 33 475 487 10.1016/j.it.2012.06. 003 22796170
61. Rapamycin in transplantation: a review of the evidence. Saunders RN, Metcalfe MS, Nicholson ML, Kidney Int 2001 59 3 16 10.1046/j.1523-1755.2001. 00460.x 11135052 (Pubitemid 32055209)
62. Autophagy signaling in cancer and its potential as novel target to improve anticancer therapy. Moretti L, Yang ES, Kim KW, Lu B, Drug Resist Updat 2007 10 135 143 10.1016/j.drup.2007.05.001 17627865 (Pubitemid 47454724)
63. The early autophagic pathway is activated by hepatitis B virus and required for viral DNA replication. Sir D, Tian Y, Chen WL, Ann DK, Yen TS, Ou JH, Proc Natl Acad Sci U S A 2010 107 4383 4388 10.1073/pnas.0911373107 20142477
64. The autophagy machinery is required to initiate hepatitis C virus replication. Dreux M, Gastaminza P, Wieland SF, Chisari FV, Proc Natl Acad Sci U S A 2009 106 14046 14051 10.1073/pnas.0907344106 19666601
65. Subversion of cellular autophagosomal machinery by RNA viruses. Jackson WT, Giddings TH Jr, Taylor MP, Mulinyawe S, Rabinovitch M, Kopito RR, Kirkegaard K, PLoS Biol 2005 3 156 10.1371/journal.pbio.0030156 15884975 (Pubitemid 40958407)
66. Current development of mTOR inhibitors as anticancer agents. Faivre S, Kroemer G, Raymond E, Nat Rev Drug Discov 2006 5 671 688 10.1038/nrd2062 16883305 (Pubitemid 44151605)
67. Rapamycin-mediated inhibition of mammalian target of rapamycin in skeletal muscle cells reduces glucose utilization and increases fatty acid oxidation. Sipula IJ, Brown NF, Perdomo G, Metabolism 2006 55 1637 1644 10.1016/j.metabol.2006.08.002 17142137 (Pubitemid 44827130)
68. Changes in tumor metabolism as readout for Mammalian target of rapamycin kinase inhibition by rapamycin in glioblastoma. Wei LH, Su H, Hildebrandt IJ, Phelps ME, Czernin J, Weber WA, Clin Cancer Res 2008 14 3416 3426 10.1158/1078-0432.CCR-07-1824 18519772
69. Differential effects of rapamycin on mammalian target of rapamycin signaling functions in mammalian cells. Edinger AL, Linardic CM, Chiang GG, Thompson CB, Abraham RT, Cancer Res 2003 63 8451 8460 14679009 (Pubitemid 37549501)
70. The mammalian target of rapamycin (mTOR) pathway regulates mitochondrial oxygen consumption and oxidative capacity. Schieke SM, Phillips D, McCoy JP Jr, Aponte AM, Shen RF, Balaban RS, Finkel T, J Biol Chem 2006 281 27643 27652 10.1074/jbc.M603536200 16847060 (Pubitemid 44401789)
71. mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Cunningham JT, Rodgers JT, Arlow DH, Vazquez F, Mootha VK, Puigserver P, Nature 2007 450 736 740 10.1038/nature06322 18046414 (Pubitemid 350207689)
72. Direct control of mitochondrial function by mTOR. Ramanathan A, Schreiber SL, Proc Natl Acad Sci U S A 2009 106 22229 22232 10.1073/pnas.0912074106 20080789
73. Characterization of the metabolic phenotype of rapamycin-treated CD8+ T cells with augmented ability to generate long-lasting memory cells. He S, Kato K, Jiang J, Wahl DR, Mineishi S, Fisher EM, Murasko DM, Glick GD, Zhang Y, PLoS One 2011 6 20107 10.1371/journal.pone.0020107 21611151
74. Duration of rapamycin treatment has differential effects on metabolism in mice. Fang Y, Westbrook R, Hill C, Boparai RK, Arum O, Spong A, Wang F, Javors MA, Chen J, Sun LY, Bartke A, Cell Metab 2013 17 456 462 10.1016/j.cmet.2013.02. 008 23473038
75. Glucose uptake and lactic acid production of adenovirus type 5-infected HEp-2 cells cultured under exponential growth and stationary phase conditions. Bardell D, Microbios 1977 20 139 144 617828 (Pubitemid 9084141)
76. Viral effects on metabolism: changes in glucose and glutamine utilization during human cytomegalovirus infection. Yu Y, Clippinger AJ, Alwine JC, Trends Microbiol 2011 19 360 367 10.1016/j.tim.2011.04.002 21570293
77. Dynamics of the cellular metabolome during human cytomegalovirus infection. Munger J, Bajad SU, Coller HA, Shenk T, Rabinowitz JD, PLoS Pathog 2006 2 132 10.1371/journal.ppat.0020132 17173481 (Pubitemid 46045203)
78. Rapamune (RAPA, rapamycin, sirolimus): mechanism of action immunosuppressive effect results from blockade of signal transduction and inhibition of cell cycle progression. Sehgal SN, Clin Biochem 1998 31 335 340 10.1016/S0009-9120(98)00045-9 9721431 (Pubitemid 28385231)
79. Regulation of cell growth and cyclin D1 expression by the constitutively active FRAP-p70s6K pathway in human pancreatic cancer cells. Grewe M, Gansauge F, Schmid RM, Adler G, Seufferlein T, Cancer Res 1999 59 3581 3587 10446965 (Pubitemid 29381856)
80. Rapamycin inhibits cdk4 activation, p21(WAF1/CIP1) expression and G1-phase progression in transformed mouse fibroblasts. Gaben AM, Saucier C, Bedin M, Barbu V, Mester J, Int J Cancer 2004 108 200 206 10.1002/ijc.11521 14639603 (Pubitemid 37541771)
81. The upregulation of p27Kip1 by rapamycin results in G1 arrest in exponentially growing T-cell lines. Kawamata S, Sakaida H, Hori T, Maeda M, Uchiyama T, Blood 1998 91 561 569 9427710 (Pubitemid 28053379)