International Journal of Radiation Oncology * Biology * Physics
Volume 66, Issue 3 , Pages 637-646 , 1 November 2006

ReVOLT: radiation-enhanced viral oncolytic therapy

  • Sunil J. Advani, M.D.

      Affiliations

    • Department of Radiation and Cellular Oncology, the University of Chicago, Chicago, IL
    • ,
  • James J. Mezhir, M.D.

      Affiliations

    • Department of Surgery, the University of Chicago, Chicago, IL
    • ,
  • Bernard Roizman, Sc.D.

      Affiliations

    • Marjorie B. Kovler Viral Oncology Laboratories, the University of Chicago, Chicago, IL
    • ,
  • Ralph R. Weichselbaum, M.D.

      Affiliations

    • Department of Radiation and Cellular Oncology, the University of Chicago, Chicago, IL
    • Corresponding Author InformationReprint requests to: Ralph R. Weichselbaum, M.D., Department of Radiation and Cellular Oncology, The University of Chicago Hospitals, Center for Advanced Medicine, Room 1329, Mail Code 9006, 5758 South Maryland Avenue, Chicago, IL 60637. Tel: (773) 702-0817; Fax: (773) 834-7233

Received 4 April 2006 ,Revised 15 June 2006 ,Accepted 16 June 2006.

References 

  1. Advani S , Weichselbaum RR , Kufe DW . Cancer gene therapy . In:  Kufe DW ,  Pollock RE ,  Weichselbaum RR , et al. editor. Cancer medicine . Hamilton, Ontario, Canada: B.C. Decker; 2003;p. 981–997
  2. Chiocca EA . Oncolytic viruses . Nat Rev Cancer . 2002;2:938–950
  3. Everts B , van der Poel HG . Replication-selective oncolytic viruses in the treatment of cancer . Cancer Gene Ther . 2005;12:141–161
  4. Kirn D . Clinical research results with dl1520 (Onyx-015), a replication-selective adenovirus for the treatment of cancer: What have we learned? . Gene Ther . 2001;8:89–98
  5. Markert JM , Medlock MD , Rabkin SD , et al.   Conditionally replicating herpes simplex virus mutant, G207 for the treatment of malignant glioma: Results of a phase I trial . Gene Ther . 2000;7:867–874
  6. Shah AC , Benos D , Gillespie GY , Markert JM . Oncolytic viruses: Clinical applications as vectors for the treatment of malignant gliomas . J Neurooncol . 2003;65:203–226
  7. Aghi M , Martuza RL . Oncolytic viral therapies—the clinical experience . Oncogene . 2005;24:7802–7816
  8. Advani SJ , Weichselbaum RR . Regional gene therapy: Principles and progress in replication-competent tumor-selective viruses . In:  Devita HS ,  Rosenberg S editor. Progress in oncology . Jones and Bartlett; 2002;p. 54–80
  9. Norman KL , Lee PW . Not all viruses are bad guys: The case for reovirus in cancer therapy . Drug Discov Today . 2005;10:847–855
  10. Stanziale SF , Fong Y . Novel approaches to cancer therapy using oncolytic viruses . Curr Mol Med . 2003;3:61–71
  11. Martuza RL , Malick A , Markert JM , et al.   Experimental therapy of human glioma by means of a genetically engineered virus mutant . Science . 1991;252:854–856
  12. Chou J , Kern ER , Whitley RJ , Roizman B . Mapping of herpes simplex virus-1 neurovirulence to gamma 134.5, a gene nonessential for growth in culture . Science . 1990;250:1262–1266
  13. He B , Chou J , Liebermann DA , et al.   The carboxyl terminus of the murine MyD116 gene substitutes for the corresponding domain of the gamma(1)34.5 gene of herpes simplex virus to preclude the premature shutoff of total protein synthesis in infected human cells . J Virol . 1996;70:84–90
  14. Chambers R , Gillespie GY , Soroceanu L , et al.   Comparison of genetically engineered herpes simplex viruses for the treatment of brain tumors in a scid mouse model of human malignant glioma . Proc Natl Acad Sci USA . 1995;92:1411–1415
  15. Mohr I , Sternberg D , Ward S , et al.   A herpes simplex virus type 1 gamma34.5 second-site suppressor mutant that exhibits enhanced growth in cultured glioblastoma cells is severely attenuated in animals . J Virol . 2001;75:5189–5196
  16. Mineta T , Rabkin SD , Yazaki T , et al.   Attenuated multi-mutated herpes simplex virus-1 for the treatment of malignant gliomas . Nat Med . 1995;1:938–943
  17. Meignier B , Longnecker R , Roizman B . In vivo behavior of genetically engineered herpes simplex viruses R7017 and R7020: Construction and evaluation in rodents . J Infect Dis . 1988;158:602–614
  18. Meignier B , Martin B , Whitley RJ , Roizman B . In vivo behavior of genetically engineered herpes simplex viruses R7017 and R7020 (II. Studies in immunocompetent and immunosuppressed owl monkeys (Aotus trivirgatus)) . J Infect Dis . 1990;162:313–321
  19. Advani SJ , Chung SM , Yan SY , et al.   Replication-competent, nonneuroinvasive genetically engineered herpes virus is highly effective in the treatment of therapy-resistant experimental human tumors . Cancer Res . 1999;59:2055–2058
  20. Chung SM , Advani SJ , Bradley JD , et al.   The use of a genetically engineered herpes simplex virus (R7020) with ionizing radiation for experimental hepatoma . Gene Ther . 2002;9:75–80
  21. Bennett JJ , Delman KA , Burt BM , et al.   Comparison of safety, delivery, and efficacy of two oncolytic herpes viruses (G207 and NV1020) for peritoneal cancer . Cancer Gene Ther . 2002;9:935–945
  22. Bischoff JR , Kirn DH , Williams A , et al.   An adenovirus mutant that replicates selectively in p53-deficient human tumor cells . Science . 1996;274:373–376
  23. Rothmann T , Hengstermann A , Whitaker NJ , et al.   Replication of ONYX-015, a potential anticancer adenovirus, is independent of p53 status in tumor cells . J Virol . 1998;72:9470–9478
  24. Harada JN , Berk AJ . p53-Independent and -dependent requirements for E1B-55K in adenovirus type 5 replication . J Virol . 1999;73:5333–5344
  25. Ries SJ , Brandts CH , Chung AS , et al.   Loss of p14ARF in tumor cells facilitates replication of the adenovirus mutant dl1520 (ONYX-015) . Nat Med . 2000;6:1128–1133
  26. Whyte P , Williamson NM , Harlow E . Cellular targets for transformation by the adenovirus E1A proteins . Cell . 1989;56:67–75
  27. Heise C , Hermiston T , Johnson L , et al.   An adenovirus E1A mutant that demonstrates potent and selective systemic anti-tumoral efficacy . Nat Med . 2000;6:1134–1139
  28. Fueyo J , Gomez-Manzano C , Alemany R , et al.   A mutant oncolytic adenovirus targeting the Rb pathway produces anti-glioma effect in vivo . Oncogene . 2000;19:2–12
  29. Rodriguez R , Schuur ER , Lim HY , et al.   Prostate attenuated replication competent adenovirus (ARCA) CN706: A selective cytotoxic for prostate-specific antigen-positive prostate cancer cells . Cancer Res . 1997;57:2559–2563
  30. Rampling R , Cruickshank G , Papanastassiou V , et al.   Toxicity evaluation of replication-competent herpes simplex virus (ICP 34.5 null mutant 1716) in patients with recurrent malignant glioma . Gene Ther . 2000;7:859–866
  31. Harrow S , Papanastassiou V , Harland J , et al.   HSV1716 injection into the brain adjacent to tumour following surgical resection of high-grade glioma: Safety data and long-term survival . Gene Ther . 2004;11:1648–1658
  32. Wallner KE , Galicich JH , Krol G , et al.   Patterns of failure following treatment for glioblastoma multiforme and anaplastic astrocytoma . Int J Radiat Oncol Biol Phys . 1989;16:1405–1409
  33. Advani SJ , Sibley GS , Song PY , et al.   Enhancement of replication of genetically engineered herpes simplex viruses by ionizing radiation: A new paradigm for destruction of therapeutically intractable tumors . Gene Ther . 1998;5:160–165
  34. Bradley JD , Kataoka Y , Advani S , et al.   Ionizing radiation improves survival in mice bearing intracranial high-grade gliomas injected with genetically modified herpes simplex virus . Clin Cancer Res . 1999;5:1517–1522
  35. Blank SV , Rubin SC , Coukos G , et al.   Replication-selective herpes simplex virus type 1 mutant therapy of cervical cancer is enhanced by low-dose radiation . Hum Gene Ther . 2002;13:627–639
  36. Stanziale SF , Petrowsky H , Joe JK , et al.   Ionizing radiation potentiates the antitumor efficacy of oncolytic herpes simplex virus G207 by upregulating ribonucleotide reductase . Surgery . 2002;132:353–359
  37. Chabes A , Thelander L . Controlled protein degradation regulates ribonucleotide reductase activity in proliferating mammalian cells during the normal cell cycle and in response to DNA damage and replication blocks . J Biol Chem . 2000;275:17747–17753
  38. Zhan Q , Lord KA , Alamo I , et al.   The gadd and MyD genes define a novel set of mammalian genes encoding acidic proteins that synergistically suppress cell growth . Mol Cell Biol . 1994;14:2361–2371
  39. Kim SH , Wong RJ , Kooby DA , et al.   Combination of mutated herpes simplex virus type 1 (G207 virus) with radiation for the treatment of squamous cell carcinoma of the head and neck . Eur J Cancer . 2005;41:313–322
  40. Jarnagin WR , Zager JS , Hezel M , et al.   Treatment of cholangiocarcinoma with oncolytic herpes simplex virus combined with external beam radiation therapy . Cancer Gene Ther . 2006;13:326–334
  41. Adusumilli PS , Stiles BM , Chan MK , et al.   Radiation therapy potentiates effective oncolytic viral therapy in the treatment of lung cancer . Ann Thorac Surg . 2005;80:409–417
  42. Bennett JJ , Adusumilli P , Petrowsky H , et al.   Up-regulation of GADD34 mediates the synergistic anticancer activity of mitomycin C and a gamma134.5 deleted oncolytic herpes virus (G207) . FASEB . 2004;18:1001–1003
  43. Dent P , Yacoub A , Fisher PB , et al.   MAPK pathways in radiation responses . Oncogene . 2003;22:5885–5896
  44. Zachos G , Clements B , Conner J . Herpes simplex virus type 1 infection stimulates p38/c-Jun N-terminal mitogen-activated protein kinase pathways and activates transcription factor AP-1 . J Biol Chem . 1999;274:5097–5103
  45. Zachos G , Koffa M , Preston CM , et al.   Herpes simplex virus type 1 blocks the apoptotic host cell defense mechanisms that target Bcl-2 and manipulates activation of p38 mitogen-activated protein kinase to improve viral replication . J Virol . 2001;75:2710–2728
  46. Mezhir JJ , Advani SJ , Smith KD , et al.   Ionizing radiation activates late herpes simplex virus 1 promoters via the p38 pathway in tumors treated with oncolytic viruses . Cancer Res . 2005;65:9479–9484
  47. Rogulski KR , Kim JH , Kim SH , Freytag SO . Glioma cells transduced with an Escherichia coli CD/HSV-1 TK fusion gene exhibit enhanced metabolic suicide and radiosensitivity . Hum Gene Ther . 1997;8:73–85
  48. Rogulski KR , Wing MS , Paielli DL , et al.   Double suicide gene therapy augments the antitumor activity of a replication-competent lytic adenovirus through enhanced cytotoxicity and radiosensitization . Hum Gene Ther . 2000;11:67–76
  49. Portella G , Pacelli R , Libertini S , et al.   ONYX-015 enhances radiation-induced death of human anaplastic thyroid carcinoma cells . J Clin Endocrinol Metab . 2003;88:5027–5032
  50. Lamfers ML , Grill J , Dirven CM , et al.   Potential of the conditionally replicative adenovirus Ad5-Delta24RGD in the treatment of malignant gliomas and its enhanced effect with radiotherapy . Cancer Res . 2002;62:5736–5742
  51. Chen Y , DeWeese T , Dilley J , et al.   CV706, a prostate cancer-specific adenovirus variant, in combination with radiotherapy produces synergistic antitumor efficacy without increasing toxicity . Cancer Res . 2001;61:5453–5460
  52. Zhang M , Li S , Li J , et al.   Ionizing radiation increases adenovirus uptake and improves transgene expression in intrahepatic colon cancer xenografts . Mol Ther . 2003;8:21–28
  53. Qian J , Yang J , Dragovic AF , et al.   Ionizing radiation-induced adenovirus infection is mediated by Dynamin 2 . Cancer Res . 2005;65:5493–5497
  54. Khuri FR , Nemunaitis J , Ganly I , et al.   A controlled trial of intratumoral ONYX-015, a selectively-replicating adenovirus, in combination with cisplatin and 5-fluorouracil in patients with recurrent head and neck cancer . Nat Med . 2000;6:879–885

 Support provided in part by NCI Program Project PO1 CA7193307-08, and a gift from Mr. and Mrs. Vincent W. Foglia

PII: S0360-3016(06)01111-4

doi: 10.1016/j.ijrobp.2006.06.034

International Journal of Radiation Oncology * Biology * Physics
Volume 66, Issue 3 , Pages 637-646 , 1 November 2006

Article Tools

* Image Usage & Resolution