Going viral: A review of replication-selective oncolytic adenoviruses

Oncotarget

Volumn 6, Issue 24, 2015, Pages 19976-19989

  Larson, Christopher ^a   Oronsky, Bryan ^b   Scicinski, Jan ^b   Fanger, Gary R ^b   Stirn, Meaghan ^a   Oronsky, Arnold ^c   Reid, Tony R ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b EpicentRx   (United States)

^c InterWest Partners   (United States)

Author keywords

Adenovirus; Immunotherapy; Oncology; Oncolytic virus

Indexed keywords

ANTINEOPLASTIC AGENT; CONDITIONALLY REPLICATING ADENOVIRUS; FLUOROURACIL; FOLINIC ACID; GOLNERMINOGENE PRADENOVEC; LONTUCIREV; ONCOLYTIC ADENOVIRUS; ONCOLYTIC VIRUS; ONCOS 102; RECOMBINANT GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; REPLICATION SELECTIVE ONCOLYTIC ADENOVIRUS; RRX 001; TALIMOGENE LAHERPAREPVEC; TEMOZOLOMIDE; UNCLASSIFIED DRUG;

ABSENCE OF SIDE EFFECTS; ADAPTIVE IMMUNITY; ANTINEOPLASTIC ACTIVITY; AUTOPHAGY; BRAIN METASTASIS; BRAIN RADIATION; CANCER IMMUNOTHERAPY; CANCER SURVIVAL; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL TRIAL (TOPIC); COLORECTAL CANCER; COLORECTAL METASTASIS; COMPUTER ASSISTED TOMOGRAPHY; DISTANT METASTASIS; DNA MODIFICATION; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG POTENCY; DRUG POTENTIATION; DRUG SAFETY; DRUG SELECTIVITY; DRUG TOLERABILITY; FEEDBACK SYSTEM; FLU LIKE SYNDROME; GENETIC ENGINEERING; HUMAN; IMMUNE SYSTEM; IMMUNOGENICITY; IMMUNOSTIMULATION; INNATE IMMUNITY; LEUKEMIA; LYMPHADENOPATHY; LYMPHOCYTOSIS; MALIGNANT NEOPLASTIC DISEASE; MELANOMA; MESOTHELIOMA; METASTASIS; METASTATIC COLORECTAL CANCER; NONHUMAN; ONCOLYTIC VIROTHERAPY; OUTCOME ASSESSMENT; OVARY CANCER; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROMOTER REGION; PROTEIN EXPRESSION; REVIEW; RISK BENEFIT ANALYSIS; SEVERE COMBINED IMMUNODEFICIENCY; SOFT TISSUE SARCOMA; SOLID TUMOR; SPLENOMEGALY; TISSUE SPECIFICITY; TREATMENT RESPONSE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS REPLICATION; ADENOVIRIDAE; ANIMAL; NEOPLASMS; PHYSIOLOGY; PROCEDURES; VIROLOGY;

ADENOVIRIDAE; ANIMALS; HUMANS; NEOPLASMS; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES;

EID: 84940192574     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5116     Document Type: Review

References (117)

1. Dock G. The influence of complicating diseases upon leukaemia. Am J Med Sci 1904; 127:561-592.
2. Pack G. Note of the experimental use of rabies vaccine for melanomatosis. Arch Dermatol Syphilol. 1950; 62:694-695.
3. Taqi AM, Abdurrahman MB, Yakubu AM and Fleming AF. Regression of Hodgkin's disease after measles. Lancet. 1981; 1:1112.
4. Bluming AZ and Ziegler JL. Regression of Burkitt's lymphoma in association with measles infection. Lancet. 1971; 2:105-106.
5. Kelly E and Russell SJ. History of Oncolytic Viruses: Genesis to Genetic Engineering. Mol Ther. 2007; 15:651-659.
6. Ring CJ. Cytolytic viruses as potential anti-cancer agents. J Gen Virol. 2002; 83:491-502.
7. Newman W and Southam CM. Virus treatment in advanced cancer; a pathological study of fifty-seven cases. Cancer. 1954; 7:106-118.
8. Southam CM and Moore AE. Induced virus infections in man by the Egypt isolates of West Nile virus. Am J Trop Med Hyg. 1954; 3:19-50.
9. Singh PK, Doley J, Kumar GR, Sahoo AP and Tiwari AK. Oncolytic viruses & their specific targeting to tumour cells. Indian J Med Res. 2012; 136:571-584.
10. Huebner RJ, Bell JA, Rowe WP, Ward TG, Suskind RG, Hartley JW and Paffenbarger RS, Jr. Studies of adenoidal-pharyngeal-conjunctival vaccines in volunteers. J Am Med Assoc. 1955; 159:986-989.
11. Zielinski T and Jordan E. [Remote results of clinical observation of the oncolytic action of adenoviruses on cervix cancer]. Nowotwory. 1969; 19:217-221.
12. Rowe WP, Huebner RJ, Gilmore LK, Parrott RH and Ward TG. Isolation of a cytopathogenic agent from human adenoids undergoing spontaneous degeneration in tissue culture. Proc Soc Exp Biol Med. 1953; 84:570-573.
13. Georgiades J, Zielinski T, Cicholska A and Jordan E. Research on the oncolytic effect of APC viruses in cancer of the cervix uteri; preliminary report. Biul Inst Med Morsk Gdansk. 1959; 10:49-57.
14. Huebner RJ, Rowe WP, Schatten WE, Smith RR and Thomas LB. Studies on the use of viruses in the treatment of carcinoma of the cervix. Cancer. 1956; 9:1211-1218.
15. Oronsky B, Carter CA, Mackie V, Scicinski J, Oronsky A, Oronsky N, Caroen S, Parker C, Lybeck M and Reid T. The war on cancer: a military perspective. Front Oncol. 2014; 4:387.
16. Hemminki A and Alvarez RD. Adenoviruses in oncology: a viable option? BioDrugs. 2002; 16:77-87.
17. Orkin SH and Motulsky AG. (1995). Report and recommendations of the panel to assess the NIH investment in research on gene therapy. In: NIH, ed.
18. Jia H and Kling J. China offers alternative gateway for experimental drugs. Nat Biotechnol. 2006; 24:117-118.
19. Liu TC and Kirn D. Gene therapy progress and prospects cancer: oncolytic viruses. Gene Ther. 2008; 15:877-884.
20. McCormick F. Success and failure on the ras pathway. Cancer Biol Ther. 2007; 6:1654-1659.
21. Garber K. China approves world's first oncolytic virus therapy for cancer treatment. J Natl Cancer Inst. 2006; 98:298-300.
22. Theodore F. (2012). Methods in Enzymology. In: Theodore F, ed. Methods in Enzymology: Academic Press), pp. xxi-l.
23. Friedman GK, Cassady KA, Beierle EA, Markert JM and Gillespie GY. Targeting pediatric cancer stem cells with oncolytic virotherapy. Pediatr Res. 2012; 71:500-510.
24. Wollmann G, Ozduman K and van den Pol AN. Oncolytic virus therapy for glioblastoma multiforme: concepts and candidates. Cancer J. 2012; 18:69-81.
25. Van Etten JL, Lane LC and Dunigan DD. DNA viruses: the really big ones (giruses). Annu Rev Microbiol. 2010; 64:83-99.
26. Liu BL, Robinson M, Han ZQ, Branston RH, English C, Reay P, McGrath Y, Thomas SK, Thornton M, Bullock P, Love CA and Coffin RS. ICP34.5 deleted herpes simplex virus with enhanced oncolytic, immune stimulating, and anti-tumour properties. Gene Ther. 2003; 10:292-303.
27. Kaufman HL, Kim DW, DeRaffele G, Mitcham J, Coffin RS and Kim-Schulze S. Local and distant immunity induced by intralesional vaccination with an oncolytic herpes virus encoding GM-CSF in patients with stage IIIc and IV melanoma. Ann Surg Oncol. 2010; 17:718-730.
28. Hu JC, Coffin RS, Davis CJ, Graham NJ, Groves N, Guest PJ, Harrington KJ, James ND, Love CA, McNeish I, Medley LC, Michael A, Nutting CM, Pandha HS, Shorrock CA, Simpson J, et al. A phase I study of OncoVEXGM-CSF, a second-generation oncolytic herpes simplex virus expressing granulocyte macrophage colony-stimulating factor. Clin Cancer Res. 2006; 12:6737-6747.
29. Senzer NN, Kaufman HL, Amatruda T, Nemunaitis M, Reid T, Daniels G, Gonzalez R, Glaspy J, Whitman E, Harrington K, Goldsweig H, Marshall T, Love C, Coffin R and Nemunaitis JJ. Phase II clinical trial of a granulocyte-macrophage colony-stimulating factor-encoding, second-generation oncolytic herpesvirus in patients with unresectable metastatic melanoma. J Clin Oncol. 2009; 27:5763-5771.
30. Harrington KJ, Hingorani M, Tanay MA, Hickey J, Bhide SA, Clarke PM, Renouf LC, Thway K, Sibtain A, McNeish IA, Newbold KL, Goldsweig H, Coffin R and Nutting CM. Phase I/II study of oncolytic HSV GM-CSF in combination with radiotherapy and cisplatin in untreated stage III/IV squamous cell cancer of the head and neck. Clin Cancer Res. 2010; 16:4005-4015.
31. Andtbacka RH, Kaufman HL, Collichio F, Amatruda T, Senzer N, Chesney J, Delman KA, Spitler LE, Puzanov I, Agarwala SS, Milhem M, Cranmer L, Curti B, Lewis K, Ross M, Guthrie T, et al. Talimogene Laherparepvec Improves Durable Response Rate in Patients With Advanced Melanoma. J Clin Oncol. 2015.
32. Mastrangelo MJ, Maguire HC, Jr., Eisenlohr LC, Laughlin CE, Monken CE, McCue PA, Kovatich AJ and Lattime EC. Intratumoral recombinant GM-CSF-encoding virus as gene therapy in patients with cutaneous melanoma. Cancer Gene Ther. 1999; 6:409-422.
33. Hwang TH, Moon A, Burke J, Ribas A, Stephenson J, Breitbach CJ, Daneshmand M, De Silva N, Parato K, Diallo JS, Lee YS, Liu TC, Bell JC and Kirn DH. A mechanistic proof-of-concept clinical trial with JX-594, a targeted multi-mechanistic oncolytic poxvirus, in patients with metastatic melanoma. Mol Ther. 2011; 19:1913-1922.
34. Park BH, Hwang T, Liu TC, Sze DY, Kim JS, Kwon HC, Oh SY, Han SY, Yoon JH, Hong SH, Moon A, Speth K, Park C, Ahn YJ, Daneshmand M, Rhee BG, et al. Use of a targeted oncolytic poxvirus, JX-594, in patients with refractory primary or metastatic liver cancer: a phase I trial. Lancet Oncol. 2008; 9:533-542.
35. Breitbach CJ, Burke J, Jonker D, Stephenson J, Haas AR, Chow LQ, Nieva J, Hwang TH, Moon A, Patt R, Pelusio A, Le Boeuf F, Burns J, Evgin L, De Silva N, Cvancic S, et al. Intravenous delivery of a multi-mechanistic cancer-targeted oncolytic poxvirus in humans. Nature. 2011; 477:99-102.
36. Heo J, Reid T, Ruo L, Breitbach CJ, Rose S, Bloomston M, Cho M, Lim HY, Chung HC, Kim CW, Burke J, Lencioni R, Hickman T, Moon A, Lee YS, Kim MK, et al. Randomized dose-finding clinical trial of oncolytic immunotherapeutic vaccinia JX-594 in liver cancer. Nat Med. 2013; 19:329-336.
37. Strong JE, Coffey MC, Tang D, Sabinin P and Lee PW. The molecular basis of viral oncolysis: usurpation of the Ras signaling pathway by reovirus. EMBO J. 1998; 17(12):3351-3362.
38. Kelly KR, Espitia CM, Mahalingam D, Oyajobi BO, Coffey M, Giles FJ, Carew JS and Nawrocki ST. Reovirus therapy stimulates endoplasmic reticular stress, NOXA induction, and augments bortezomib-mediated apoptosis in multiple myeloma. Oncogene. 2012; 31:3023-3038.
39. Vidal L, Pandha HS, Yap TA, White CL, Twigger K, Vile RG, Melcher A, Coffey M, Harrington KJ and DeBono JS. A phase I study of intravenous oncolytic reovirus type 3 Dearing in patients with advanced cancer. Clin Cancer Res. 2008; 14:7127-7137.
40. Gollamudi R, Ghalib MH, Desai KK, Chaudhary I, Wong B, Einstein M, Coffey M, Gill GM, Mettinger K, Mariadason JM, Mani S and Goel S. Intravenous administration of Reolysin, a live replication competent RNA virus is safe in patients with advanced solid tumors. Invest New Drugs. 2010; 28:641-649.
41. Galanis E, Markovic SN, Suman VJ, Nuovo GJ, Vile RG, Kottke TJ, Nevala WK, Thompson MA, Lewis JE, Rumilla KM, Roulstone V, Harrington K, Linette GP, Maples WJ, Coffey M, Zwiebel J, et al. Phase II trial of intravenous administration of Reolysin((R)) (Reovirus Serotype-3-dearing Strain) in patients with metastatic melanoma. Mol Ther. 2012; 20:1998-2003.
42. Morris DG, Feng X, DiFrancesco LM, Fonseca K, Forsyth PA, Paterson AH, Coffey MC and Thompson B. REO-001: A phase I trial of percutaneous intralesional administration of reovirus type 3 dearing (Reolysin(R)) in patients with advanced solid tumors. Invest New Drugs. 2013; 31:696-706.
43. Forsyth P, Roldan G, George D, Wallace C, Palmer CA, Morris D, Cairncross G, Matthews MV, Markert J, Gillespie Y, Coffey M, Thompson B and Hamilton M. A phase I trial of intratumoral administration of reovirus in patients with histologically confirmed recurrent malignant gliomas. Mol Ther. 2008; 16:627-632.
44. Lolkema MP, Arkenau HT, Harrington K, Roxburgh P, Morrison R, Roulstone V, Twigger K, Coffey M, Mettinger K, Gill G, Evans TR and de Bono JS. A phase I study of the combination of intravenous reovirus type 3 Dearing and gemcitabine in patients with advanced cancer. Clin Cancer Res. 2011; 17:581-588.
45. Comins C, Spicer J, Protheroe A, Roulstone V, Twigger K, White CM, Vile R, Melcher A, Coffey MC, Mettinger KL, Nuovo G, Cohn DE, Phelps M, Harrington KJ and Pandha HS. REO-10: a phase I study of intravenous reovirus and docetaxel in patients with advanced cancer. Clin Cancer Res. 2010; 16:5564-5572.
46. Karapanagiotou EM, Roulstone V, Twigger K, Ball M, Tanay M, Nutting C, Newbold K, Gore ME, Larkin J, Syrigos KN, Coffey M, Thompson B, Mettinger K, Vile RG, Pandha HS, Hall GD, et al. Phase I/II trial of carboplatin and paclitaxel chemotherapy in combination with intravenous oncolytic reovirus in patients with advanced malignancies. Clin Cancer Res. 2012; 18:2080-2089.
47. Benko M, Harrach B and Russell W. (2000). Virus Taxonomy; Seventh Report of the International Committee on Taxonomy of Viruses. In: Van Regenmortel M, Fauquet C and Bishop D, eds. Virus Taxonomy; Seventh Report of the International Committee on Taxonomy of Viruses. (New York: Academic Press).
48. Shenk T. (1996). Adenoviridae: the viruses and their replication. In: Fields B, Knipe D and Howley P, eds. Virology. (Philadelphia: Lippencott-Raven), pp. 2111-2148.
49. Purkayastha A, Ditty SE, Su J, McGraw J, Hadfield TL, Tibbetts C and Seto D. Genomic and bioinformatics analysis of HAdV-4, a human adenovirus causing acute respiratory disease: implications for gene therapy and vaccine vector development. J Virol. 2005; 79:2559-2572.
50. Cook JL and Lewis AM, Jr. Differential NK cell and macrophage killing of hamster cells infected with nononcogenic or oncogenic adenovirus. Science. 1984; 224:612-615.
51. Williams PD, Ranjzad P, Kakar SJ and Kingston PA. Development of viral vectors for use in cardiovascular gene therapy. Viruses. 2010; 2:334-371.
52. Schoggins JW and Falck-Pedersen E. Fiber and penton base capsid modifications yield diminished adenovirus type 5 transduction and proinflammatory gene expression with retention of antigen-specific humoral immunity. J Virol. 2006; 80:10634-10644.
53. Trotman LC, Mosberger N, Fornerod M, Stidwill RP and Greber UF. Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1. Nat Cell Biol. 2001; 3:1092-1100.
54. Chakraborty AA and Tansey WP. Adenoviral E1A function through Myc. Cancer Res. 2009; 69:6-9.
55. Frisch SM and Mymryk JS. Adenovirus-5 E1A: paradox and paradigm. Nat Rev Mol Cell Biol. 2002; 3:441-452.
56. Nemajerova A, Talos F, Moll UM and Petrenko O. Rb function is required for E1A-induced S-phase checkpoint activation. Cell Death Differ. 2008; 15:1440-1449.
57. Dynlacht BD. E2F and p53 make a nice couple: converging pathways in apoptosis. Cell Death Differ. 2005; 12:313-314.
58. Berk AJ. Recent lessons in gene expression, cell cycle control, and cell biology from adenovirus. Oncogene. 2005; 24:7673-7685.
59. Rao L, Debbas M, Sabbatini P, Hockenbery D, Korsmeyer S and White E. The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kDa and Bcl-2 proteins. Proc Natl Acad Sci U S A. 1992; 89:7742-7746.
60. Harada JN and Berk AJ. p53-Independent and-dependent requirements for E1B-55K in adenovirus type 5 replication. J Virol. 1999; 73:5333-5344.
61. McCormick F. ONYX-015 selectivity and the p14ARF pathway. Oncogene. 2000; 19:6670-6672.
62. Goodrum FD and Ornelles DA. p53 status does not determine outcome of E1B 55-kilodalton mutant adenovirus lytic infection. J Virol. 1998; 72:9479-9490.
63. Au T, Thorne S, Korn WM, Sze D, Kirn D and Reid TR. Minimal hepatic toxicity of Onyx-015: spatial restriction of coxsackie-adenoviral receptor in normal liver. Cancer Gene Ther. 2007; 14:139-150.
64. Nagata K, Guggenheimer RA and Hurwitz J. Specific binding of a cellular DNA replication protein to the origin of replication of adenovirus DNA. Proc Natl Acad Sci U S A. 1983; 80:6177-6181.
65. Burgert HG and Kvist S. The E3/19K protein of adenovirus type 2 binds to the domains of histocompatibility antigens required for CTL recognition. EMBO J. 1987; 6:2019-2026.
66. Deryckere F and Burgert HG. Tumor necrosis factor alpha induces the adenovirus early 3 promoter by activation of NF-kappaB. J Biol Chem. 1996; 271:30249-30255.
67. Halbert DN, Cutt JR and Shenk T. Adenovirus early region 4 encodes functions required for efficient DNA replication, late gene expression, and host cell shutoff. J Virol. 1985; 56:250-257.
68. Harada JN, Shevchenko A, Shevchenko A, Pallas DC and Berk AJ. Analysis of the adenovirus E1B-55K-anchored proteome reveals its link to ubiquitination machinery. J Virol. 2002; 76:9194-9206.
69. Gonzalez RA and Flint SJ. Effects of mutations in the adenoviral E1B 55-kilodalton protein coding sequence on viral late mRNA metabolism. J Virol. 2002; 76:4507-4519.
70. Farley DC, Brown JL and Leppard KN. Activation of the early-late switch in adenovirus type 5 major late transcription unit expression by L4 gene products. J Virol. 2004; 78:1782-1791.
71. Kochanek S. (2009). Adenovirus. In: Schwab M, ed. Encyclopedia of Cancer. (Berlin: Springer), pp. 50-53.
72. Abou El Hassan MA, van der Meulen-Muileman I, Abbas S and Kruyt FA. Conditionally replicating adenoviruses kill tumor cells via a basic apoptotic machinery-independent mechanism that resembles necrosis-like programmed cell death. J Virol. 2004; 78:12243-12251.
73. Kanaya T, Kyo S, Hamada K, Takakura M, Kitagawa Y, Harada H and Inoue M. Adenoviral expression of p53 represses telomerase activity through down-regulation of human telomerase reverse transcriptase transcription. Clin Cancer Res. 2000; 6:1239-1247.
74. Small EJ, Carducci MA, Burke JM, Rodriguez R, Fong L, van Ummersen L, Yu DC, Aimi J, Ando D, Working P, Kirn D and Wilding G. A phase I trial of intravenous CG7870, a replication-selective, prostate-specific antigen-targeted oncolytic adenovirus, for the treatment of hormone-refractory, metastatic prostate cancer. Mol Ther. 2006; 14:107-117.
75. Coughlan L, Vallath S, Gros A, Gimenez-Alejandre M, Van Rooijen N, Thomas GJ, Baker AH, Cascallo M, Alemany R and Hart IR. Combined fiber modifications both to target alpha(v)beta(6) and detarget the coxsackievirus-adenovirus receptor improve virus toxicity profiles in vivo but fail to improve antitumoral efficacy relative to adenovirus serotype 5. Hum Gene Ther. 2012; 23:960-979.
76. Kim KH, Dmitriev IP, Saddekni S, Kashentseva EA, Harris RD, Aurigemma R, Bae S, Singh KP, Siegal GP, Curiel DT and Alvarez RD. A phase I clinical trial of Ad5/3-Delta24, a novel serotype-chimeric, infectivity-enhanced, conditionally-replicative adenovirus (CRAd), in patients with recurrent ovarian cancer. Gynecol Oncol. 2013; 130:518-524.
77. O'Shea CC, Johnson L, Bagus B, Choi S, Nicholas C, Shen A, Boyle L, Pandey K, Soria C, Kunich J, Shen Y, Habets G, Ginzinger D and McCormick F. Late viral RNA export, rather than p53 inactivation, determines ONYX-015 tumor selectivity. Cancer Cell. 2004; 6:611-623.
78. Hacein-Bey-Abina S, Von Kalle C, Schmidt M, McCormack MP, Wulffraat N, Leboulch P, Lim A, Osborne CS, Pawliuk R, Morillon E, Sorensen R, Forster A, Fraser P, Cohen JI, de Saint Basile G, Alexander I, et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science. 2003; 302:415-419.
79. Raper SE, Chirmule N, Lee FS, Wivel NA, Bagg A, Gao GP, Wilson JM and Batshaw ML. Fatal systemic inflammatory response syndrome in a ornithine transcarbamylase deficient patient following adenoviral gene transfer. Mol Genet Metab. 2003; 80:148-158.
80. Savulescu J. Harm, ethics committees and the gene therapy death. J Med Ethics. 2001; 27:148-150.
81. Reid T, Warren R and Kirn D. Intravascular adenoviral agents in cancer patients: lessons from clinical trials. Cancer Gene Ther. 2002; 9:979-986.
82. Ganly I, Kirn D, Eckhardt G, Rodriguez GI, Soutar DS, Otto R, Robertson AG, Park O, Gulley ML, Heise C, Von Hoff DD and Kaye SB. A phase I study of Onyx-015, an E1B attenuated adenovirus, administered intratumorally to patients with recurrent head and neck cancer. Clin Cancer Res. 2000; 6:798-806.
83. Griesenbach U. Progress and Prospects: Gene Therapy Clinical Trials (Part 2). Gene Ther. 2007; 14:1555-1563.
84. Wolchok JD, Hoos A, O'Day S, Weber JS, Hamid O, Lebbe C, Maio M, Binder M, Bohnsack O, Nichol G, Humphrey R and Hodi FS. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res. 2009; 15:7412-7420.
85. Parvez K, Parvez A and Zadeh G. The diagnosis and treatment of pseudoprogression, radiation necrosis and brain tumor recurrence. Int J Mol Sci. 2014; 15:11832-11846.
86. Werewka-Maczuga A, Osinski T, Chrzan R, Buczek M and Urbanik A. Characteristics of computed tomography imaging of gastrointestinal stromal tumor (GIST) and related diagnostic problems. Pol J Radiol. 2011; 76:38-48.
87. Reid T, Infante J, Burris III H, Scribner C, Knox S, Oronsky B, Stephens J and Scicinski J. Activity observed in a phase I dose escalation trial of the hypoxia-activated, NO prodrug, RRx-001. J Clin Oncol 2013; 31(suppl 4; abstr 241).
88. Reid TR, Freeman S, Post L, McCormick F and Sze DY. Effects of Onyx-015 among metastatic colorectal cancer patients that have failed prior treatment with 5-FU/leucovorin. Cancer Gene Ther. 2005; 12:673-681.
89. Hemminki A. Oncolytic immunotherapy: where are we clinically? Scientifica (Cairo). 2014; 2014:862925.
90. Heise C, Hermiston T, Johnson L, Brooks G, Sampson-Johannes A, Williams A, Hawkins L and Kirn D. An adenovirus E1A mutant that demonstrates potent and selective systemic anti-tumoral efficacy. Nat Med. 2000; 6:1134-1139.
91. Shayakhmetov DM, Di Paolo NC and Mossman KL. Recognition of virus infection and innate host responses to viral gene therapy vectors. Mol Ther. 2010; 18:1422-1429.
92. Smith JS, Xu Z, Tian J, Palmer DJ, Ng P and Byrnes AP. The role of endosomal escape and mitogen-activated protein kinases in adenoviral activation of the innate immune response. PLoS One. 2011; 6:e26755.
93. Dummer R, Rochlitz C, Velu T, Acres B, Limacher JM, Bleuzen P, Lacoste G, Slos P, Romero P and Urosevic M. Intralesional adenovirus-mediated interleukin-2 gene transfer for advanced solid cancers and melanoma. Mol Ther. 2008; 16:985-994.
94. Rasmussen H, Rasmussen C, Lempicki M, Durham R, Brough D, King CR and Weichselbaum R. TNFerade Biologic: preclinical toxicology of a novel adenovector with a radiation-inducible promoter, carrying the human tumor necrosis factor alpha gene. Cancer Gene Ther. 2002; 9:951-957.
95. MacGill RS, Davis TA, Macko J, Mauceri HJ, Weichselbaum RR and King CR. Local gene delivery of tumor necrosis factor alpha can impact primary tumor growth and metastases through a host-mediated response. Clin Exp Metastasis. 2007; 24:521-531.
96. Herman JM, Wild AT, Wang H, Tran PT, Chang KJ, Taylor GE, Donehower RC, Pawlik TM, Ziegler MA, Cai H, Savage DT, Canto MI, Klapman J, Reid T, Shah RJ, Hoffe SE, et al. Randomized phase III multi-institutional study of TNFerade biologic with fluorouracil and radiotherapy for locally advanced pancreatic cancer: final results. J Clin Oncol. 2013; 31:886-894.
97. Malmstrom PU, Loskog AS, Lindqvist CA, Mangsbo SM, Fransson M, Wanders A, Gardmark T and Totterman TH. AdCD40L immunogene therapy for bladder carcinoma-the first phase I/IIa trial. Clin Cancer Res. 2010; 16:3279-3287.
98. Castro JE, Melo-Cardenas J, Urquiza M, Barajas-Gamboa JS, Pakbaz RS and Kipps TJ. Gene immunotherapy of chronic lymphocytic leukemia: a phase I study of intranodally injected adenovirus expressing a chimeric CD154 molecule. Cancer Res. 2012; 72:2937-2948.
99. Dranoff G, Jaffee E, Lazenby A, Golumbek P, Levitsky H, Brose K, Jackson V, Hamada H, Pardoll D and Mulligan RC. Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc Natl Acad Sci U S A. 1993; 90:3539-3543.
100. Cerullo V, Pesonen S, Diaconu I, Escutenaire S, Arstila PT, Ugolini M, Nokisalmi P, Raki M, Laasonen L, Sarkioja M, Rajecki M, Kangasniemi L, Guse K, Helminen A, Ahtiainen L, Ristimaki A, et al. Oncolytic adenovirus coding for granulocyte macrophage colony-stimulating factor induces antitumoral immunity in cancer patients. Cancer Res. 2010; 70:4297-4309.
101. Majumder M, Kumar A, Heckman C, Kankainen M, Pesonen S, Jäger E, Karbach J, Joensuu T, Kairemo K, Partanen K, Alanko T, Hemminki A, Backman C, Dienel K, von Euler M, Hakonen T, et al. Gene expression analysis of tumors demonstrates an induction of Th1 type immune response following intratumoral administration of ONCOS-102 in refractory solid tumor patients. Journal for Immunotherapy of Cancer. 2014; 2:P230-P230.
102. Ferguson MS, Lemoine NR and Wang Y. Systemic delivery of oncolytic viruses: hopes and hurdles. Adv Virol. 2012; 2012:805629.
103. O'Riordan CR, Lachapelle A, Delgado C, Parkes V, Wadsworth SC, Smith AE and Francis GE. PEGylation of adenovirus with retention of infectivity and protection from neutralizing antibody in vitro and in vivo. Hum Gene Ther. 1999; 10:1349-1358.
104. Bolhassani A, Javanzad S, Saleh T, Hashemi M, Aghasadeghi MR and Sadat SM. Polymeric nanoparticles: potent vectors for vaccine delivery targeting cancer and infectious diseases. Hum Vaccin Immunother. 2014; 10:321-332.
105. Wojton J and Kaur B. Impact of tumor microenvironment on oncolytic viral therapy. Cytokine Growth Factor Rev. 2010; 21:127-134.
106. Dhar D, Toth K and Wold WS. Cycles of transient high-dose cyclophosphamide administration and intratumoral oncolytic adenovirus vector injection for long-term tumor suppression in Syrian hamsters. Cancer Gene Ther. 2014; 21:171-178.
107. Siva S, MacManus MP, Martin RF and Martin OA. Abscopal effects of radiation therapy: a clinical review for the radiobiologist. Cancer Lett. 2015; 356:82-90.
108. Bell J. Oncolytic viruses: immune or cytolytic therapy? Mol Ther. 2014; 22:1231-1232.
109. Koski A, Kangasniemi L, Escutenaire S, Pesonen S, Cerullo V, 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; 18:1874-1884.
110. Errington F, Steele L, Prestwich R, Harrington KJ, Pandha HS, Vidal L, de Bono J, Selby P, Coffey M, Vile R and Melcher A. Reovirus activates human dendritic cells to promote innate antitumor immunity. J Immunol. 2008; 180:6018-6026.
111. Cerullo V, Diaconu I, Kangasniemi L, Rajecki M, Escutenaire S, Koski A, Romano V, Rouvinen N, Tuuminen T, Laasonen L, Partanen K, Kauppinen S, Joensuu T, Oksanen M, Holm SL, Haavisto E, et al. Immunological effects of low-dose cyclophosphamide in cancer patients treated with oncolytic adenovirus. Mol Ther. 2011; 19:1737-1746.
112. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, Evdemon-Hogan M, Conejo-Garcia JR, Zhang L, Burow M, Zhu Y, Wei S, Kryczek I, Daniel B, Gordon A, Myers L, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med. 2004; 10:942-949.
113. Liikanen I, Ahtiainen L, Hirvinen ML, Bramante S, Cerullo V, Nokisalmi P, Hemminki O, Diaconu I, Pesonen S, Koski A, Kangasniemi L, Pesonen SK, Oksanen M, Laasonen L, Partanen K, Joensuu T, et al. Oncolytic adenovirus with temozolomide induces autophagy and antitumor immune responses in cancer patients. Mol Ther. 2013; 21:1212-1223.
114. Ning S, Bednarski M, Oronsky B, Scicinski J, Saul G and Knox SJ. Dinitroazetidines are a novel class of anticancer agents and hypoxia-activated radiation sensitizers developed from highly energetic materials. Cancer Res. 2012; 72:2600-2608.
115. Reid T, Dad S, Korn R, Oronsky B, Knox S and Scicinski J. Two Case Reports of Resensitization to Previous Chemotherapy with the Novel Hypoxia-Activated Hypomethylating Anticancer Agent RRx-001 in Metastatic Colorectal Cancer Patients. Case Rep Oncol. 2014; 7:79-85.
116. Derynck R, Goeddel DV, Ullrich A, Gutterman JU, Williams RD, Bringman TS and Berger WH. Synthesis of messenger RNAs for transforming growth factors alpha and beta and the epidermal growth factor receptor by human tumors. Cancer Res. 1987; 47:707-712.
117. Smith JG, Wiethoff CM, Stewart PL and Nemerow GR. Adenovirus. Curr Top Microbiol Immunol. 2010; 343:195-224.