Concurrent chemotherapy inhibits herpes simplex virus-1 replication and oncolysis

Cancer Gene Therapy

Volumn 20, Issue 2, 2013, Pages 133-140

  Kulu, Y ^a   Kawasaki, H ^a   Donahue, J M ^a   Kasuya, H ^a   Cusack, J C ^a   Choi, E W ^a   Kuruppu, D K ^a   Fuchs, B C ^a   Tanabe, K K ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

chemotherapeutics; combination therapy; Herpes simplex virus; oncolytic HSV; viral oncolysis

Indexed keywords

FLUOROURACIL; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INITIATION FACTOR 2ALPHA; IRINOTECAN; METHOTREXATE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CANCER CELL; COLON CANCER; DEPHOSPHORYLATION; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; VIRAL ONCOLYSIS; VIRUS INHIBITION; VIRUS REPLICATION;

CAMPTOTHECIN; CELL LINE, TUMOR; COLONIC NEOPLASMS; COMBINED MODALITY THERAPY; FLUOROURACIL; HERPESVIRUS 1, HUMAN; HUMANS; METHOTREXATE; NF-KAPPA B; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; PANCREATIC NEOPLASMS; TRANSCRIPTIONAL ACTIVATION; TUMOR NECROSIS FACTOR-ALPHA; VIRUS REPLICATION;

EUKARYOTA; HUMAN HERPESVIRUS 1; SIMPLEXVIRUS;

EID: 84874110140     PISSN: 09291903     EISSN: 14765500     Source Type: Journal    
DOI: 10.1038/cgt.2012.97     Document Type: Article

References (65)

1. Carroll NM, Chiocca EA, Takahashi K, Tanabe KK. Enhancement of gene therapy specificity for diffuse colon carcinoma liver metastases with recombinant herpes simplex virus. Ann Surg 1996; 224: 323-329.
2. Pawlik TM, Nakamura H, Yoon SS, Mullen JT, Chandrasekhar S, Chiocca EA et al. Oncolysis of diffuse hepatocellular carcinoma by intravascular administration of a replication-competent, genetically engineered herpesvirus. Cancer Res 2000; 60: 2790-2795.
3. Yoon SS, Nakamura H, Carroll NM, Bode BP, Chiocca EA, Tanabe KK. An oncolytic herpes simplex virus type 1 selectively destroys diffuse liver metastases from colon carcinoma. FASEB J 2000; 14: 301-311.
4. Mullen JT, Donahue JM, Chandrasekhar S, Yoon SS, Liu W, Ellis LM et al. Oncolysis by viral replication and inhibition of angiogenesis by a replication-conditional herpes simplex virus that expresses mouse endostatin. Cancer 2004; 101: 869-877.
5. Nakamura H, Mullen JT, Chandrasekhar S, Pawlik TM, Yoon SS, Tanabe KK. Multimodality therapy with a replication-conditional herpes simplex virus 1 mutant that expresses yeast cytosine deaminase for intratumoral conversion of 5-fluorocytosine to 5-fluorouracil. Cancer Res 2001; 61: 5447-5452.
6. Nakamura H, Kasuya H, Mullen JT, Yoon SS, Pawlik TM, Chandrasekhar S et al. Regulation of herpes simplex virus gamma(1)34.5 expression and oncolysis of diffuse liver metastases by Myb34.5. J Clin Invest 2002; 109: 871-882.
7. Geevarghese SK, Geller DA, de Haan HA, Horer M, Knoll AE, Mescheder A et al. Phase I/II study of oncolytic herpes simplex virus NV1020 in patients with extensively pretreated refractory colorectal cancer metastatic to the liver. Hum Gene Ther 2010; 21: 1119-1128.
8. Harrington KJ, Hingorani M, Tanay MA, Hickey J, Bhide SA, Clarke PM et al. 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.
9. Kaufman HL, Bines SD. OPTIM trial: a Phase III trial of an oncolytic herpes virus encoding GM-CSF for unresectable stage III or IV melanoma. Fut Oncol 2010; 6: 941-949.
10. Gale Jr M, Katze MG. Molecular mechanisms of interferon resistance mediated by viral-directed inhibition of PKR, the interferon-induced protein kinase. Pharmacol Ther 1998; 78: 29-46.
11. He B, Gross M, Roizman B. The gamma(1)34.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1alpha to dephosphorylate the alpha subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNA-activated protein kinase. Proc Natl Acad Sci USA 1997; 94: 843-848.
12. Jacobs BL, Langland JO. When two strands are better than one: the mediators and modulators of the cellular responses to double-stranded RNA. Virology 1996; 219: 339-349.
13. 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.
14. Chou J, Roizman B. The gamma 1(34.5) gene of herpes simplex virus 1 precludes neuroblastoma cells from triggering total shutoff of protein synthesis characteristic of programed cell death in neuronal cells. Proc Natl Acad Sci USA 1992; 89: 3266-3270.
15. He B, Gross M, Roizman B. The gamma134.5 protein of herpes simplex virus 1 has the structural and functional attributes of a protein phosphatase 1 regulatory subunit and is present in a high molecular weight complex with the enzyme in infected cells. J Biol Chem 1998; 273: 20737-20743.
16. Hiscott J, Kwon H, Genin P. Hostile takeovers: viral appropriation of the NF-kappaB pathway. J Clin Invest 2001; 107: 143-151.
17. Wang CY, Mayo MW, Baldwin Jr. AS. TNF-and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB. Science 1996; 274: 784-787.
18. Majumdar S, Aggarwal BB. Methotrexate suppresses NF-kappaB activation through inhibition of IkappaBalpha phosphorylation and degradation. J Immunol 2001; 167: 2911-2920.
19. Cai WZ, Schaffer PA. Herpes simplex virus type 1 ICP0 plays a critical role in the de novo synthesis of infectious virus following transfection of viral DNA. J Virol 1989; 63: 4579-4589.
20. Liu ZQ, Kunimatsu M, Yang JP, Ozaki Y, Sasaki M, Okamoto T. Proteolytic processing of nuclear factor kappa B by calpain in vitro. FEBS Lett 1996; 385: 109-113.
21. Oeckinghaus A, Hayden MS, Ghosh S. Crosstalk in NF-kappaB signaling pathways. Nat Immunol 2011; 12: 695-708.
22. Roberts KL, Baines JD. UL31 of herpes simplex virus 1 is necessary for optimal NF-kappaB activation and expression of viral gene products. J Virol 2011; 85: 4947-4953.
23. Shepard AA, Imbalzano AN, DeLuca NA. Separation of primary structural components conferring autoregulation, transactivation, and DNA-binding properties to the herpes simplex virus transcriptional regulatory protein ICP4. J Virol 1989; 63: 3714-3728.
24. Goldstein DJ, Weller SK. Factor(s) present in herpes simplex virus type 1-infected cells can compensate for the loss of the large subunit of the viral ribonucleotide reductase: characterization of an ICP6 deletion mutant. Virology 1988; 166: 41-51.
25. Rice SA, Knipe DM. Genetic evidence for two distinct transactivation functions of the herpes simplex virus alpha protein ICP27. J Virol 1990; 64: 1704-1715.
26. Goldin AL, Sandri-Goldin RM, Levine M, Glorioso JC. Cloning of herpes simplex virus type 1 sequences representing the whole genome. J Virol 1981; 38: 50-58.
27. Lelie PN, Reesink HW, Lucas CJ. Inactivation of 12 viruses by heating steps applied during manufacture of a hepatitis B vaccine. J Med Virol 1987; 23: 297-301.
28. Cusack Jr JC, Liu R, Baldwin Jr AS. Inducible chemoresistance to 7-ethyl-10-[4-(1-piperidino)-1-piperidino]-carbonyloxycamptothe cin (CPT-11) in colorectal cancer cells and a xenograft model is overcome by inhibition of nuclear factor-kappaB activation. Cancer Res 2000; 60: 2323-2330.
29. Wang CY, Cusack Jr JC, Liu R, Baldwin Jr AS. Control of inducible chemoresistance: enhanced anti-tumor therapy through increased apoptosis by inhibition of NF-kappaB. Nat Med 1999; 5: 412-417.
30. Chandrasekhar S, Souba WW, Abcouwer SF. Use of modified agarose gel electrophoresis to resolve protein-DNA complexes for electrophoretic mobility shift assay. Biotechniques 1998; 24: 216-218.
31. MacKie RM, Stewart B, Brown SM. Intralesional injection of herpes simplex virus 1716 in metastatic melanoma. Lancet 2001; 357: 525-526.
32. Markert JM, Medlock MD, Rabkin SD, Gillespie GY, Todo T, Hunter WD et al. Conditionally replicating herpes simplex virus mutant, G207 for the treatment of malignant glioma: results of a phase I trial. Gene Therapy 2000; 7: 867-874.
33. Papanastassiou V, Rampling R, Fraser M, Petty R, Hadley D, Nicoll J et al. The potential for efficacy of the modified (ICP 34.5(-)) herpes simplex virus HSV1716 following intratumoural injection into human malignant glioma: a proof of principle study. Gene Therapy 2002; 9: 398-406.
34. Rampling R, Cruickshank G, Papanastassiou V, Nicoll J, Hadley D, Brennan D et al. Toxicity evaluation of replication-competent herpes simplex virus (ICP 34.5 null mutant 1716) in patients with recurrent malignant glioma. Gene Therapy 2000; 7: 859-866.
35. Abouel Hassan MA, Braam SR, Kruyt FA. Paclitaxel and vincristine potentiate adenoviral oncolysis that is associated with cell cycle and apoptosis modulation, whereas they differentially affect the viral life cycle in non-small-cell lung cancer cells. Cancer Gene Ther 2006; 13: 1105-1114.
36. Bennett JJ, Adusumilli P, Petrowsky H, Burt BM, Roberts G, Delman KA et al. Up-regulation of GADD34 mediates the synergistic anticancer activity of mitomycin C and a gamma134.5 deleted oncolytic herpes virus (G207). FASEB J 2004; 18: 1001-1003.
37. Cinatl Jr J, Cinatl J, Michaelis M, Kabickova H, Kotchetkov R, Vogel JU et al. Potent oncolytic activity of multimutated herpes simplex virus G207 in combination with vincristine against human rhabdomyosarcoma. Cancer Res 2003; 63: 1508-1514.
38. Gutermann A, Mayer E, von Dehn-Rothfelser K, Breidenstein C, Weber M, Muench M et al. Efficacy of oncolytic herpesvirus NV1020 can be enhanced by combination with chemotherapeutics in colon carcinoma cells. Hum Gene Ther 2006; 17: 1241-1253.
39. Heinemann L, Simpson GR, Boxall A, Kottke T, Relph KL, Vile R et al. Synergistic effects of oncolytic reovirus and docetaxel chemotherapy in prostate cancer. BMC Cancer 2011; 11: 221.
40. Hoffmann D, Bangen JM, Bayer W, Wildner O. Synergy between expression of fusogenic membrane proteins, chemotherapy and facultative virotherapy in colorectal cancer. Gene Therapy 2006; 13: 1534-1544.
41. Ingemarsdotter CK, Baird SK, Connell CM, Oberg D, Hallden G, McNeish IA. Lowdose paclitaxel synergizes with oncolytic adenoviruses via mitotic slippage and apoptosis in ovarian cancer. Oncogene 2010; 29: 6051-6063.
42. Kanai R, Rabkin SD, Yip S, Sgubin D, Zaupa CM, Hirose Y et al. Oncolytic virusmediated manipulation of DNA damage responses: synergy with chemotherapy in killing glioblastoma stem cells. J Natl Cancer Inst 2012; 104: 42-55.
43. Karapanagiotou EM, Roulstone V, Twigger K, Ball M, Tanay M, Nutting C et al. Phase I/II trial of carboplatin and paclitaxel chemotherapy in combination with intravenous oncolytic reovirus in patients with advanced malignancies. Clinical Cancer Res 2012; 18: 2080-2089.
44. Roulstone V, Twigger K, Zaidi S, Pencavel T, Kyula JN, White C et al. Synergistic cytotoxicity of oncolytic reovirus in combination with cisplatin-paclitaxel doublet chemotherapy. Gene Therapy 2012, doi:10.1038/gt.2012.68.
45. Sei S, Mussio JK, Yang QE, Nagashima K, Parchment RE, Coffey MC et al. Synergistic antitumor activity of oncolytic reovirus and chemotherapeutic agents in non-small cell lung cancer cells. Mol Cancer 2009; 8: 47.
46. Senzer NN, Kaufman HL, Amatruda T, Nemunaitis M, Reid T, Daniels G et al. 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.
47. Toyoizumi T, Mick R, Abbas AE, Kang EH, Kaiser LR, Molnar-Kimber KL. Combined therapy with chemotherapeutic agents and herpes simplex virus type 1 ICP34.5 mutant (HSV-1716) in human non-small cell lung cancer. Hum Gene Ther 1999; 10: 3013-3029.
48. Ungerechts G, Springfeld C, Frenzke ME, Lampe J, Johnston PB, Parker WB et al. Lymphoma chemovirotherapy: CD20-targeted and convertase-armed measles virus can synergize with fludarabine. Cancer Res 2007; 67: 10939-10947.
49. Watanabe I, Kasuya H, Nomura N, Shikano T, Shirota T, Kanazumi N et al. Effects of tumor selective replication-competent herpes viruses in combination with gemcitabine on pancreatic cancer. Cancer Chemother Pharmacol 2008; 61: 875-882.
50. Opyrchal M, Aderca I, Galanis E. Phase I clinical trial of locoregional administration of the oncolytic adenovirus ONYX-015 in combination with mitomycin-C, doxorubicin, and cisplatin chemotherapy in patients with advanced sarcomas. Methods Mol Biol (Clifton, NJ) 2009; 542: 705-717.
51. Comins C, Spicer J, Protheroe A, Roulstone V, Twigger K, White CM et al. REO-10: a phase I study of intravenous reovirus and docetaxel in patients with advanced cancer. Clinical Cancer Res 2010; 16: 5564-5572.
52. Cheema TA, Kanai R, Kim GW, Wakimoto H, Passer B, Rabkin SD et al. Enhanced antitumor efficacy of low-dose etoposide with oncolytic herpes simplex virus in human glioblastoma stem cell xenografts. Clinical Cancer Res 2011; 17: 7383-7393.
53. Passer BJ, Castelo-Branco P, Buhrman JS, Varghese S, Rabkin SD, Martuza RL. Oncolytic herpes simplex virus vectors and taxanes synergize to promote killing of prostate cancer cells. Cancer Gene Ther 2009; 16: 551-560.
54. Eisenberg DP, Adusumilli PS, Hendershott KJ, Yu Z, Mullerad M, Chan MK et al. 5-Fluorouracil and gemcitabine potentiate the efficacy of oncolytic herpes viral gene therapy in the treatment of pancreatic cancer. Journal of Gastrointest Surg 2005; 9: 1068-1077.
55. Blakley RL. Dihydrofolate Reductase in Folate and Pterins. Wiley: New York, 1984, pp 191-251.
56. Daikoku T, Yamamoto N, Maeno K, Nishiyama Y. Role of viral ribonucleotide reductase in the increase of dTTP pool size in herpes simplex virus-infected Vero cells. J Gen Virol 1991; 72(Part 6): 1441-1444.
57. Kasahara Y, Nakai Y, Miura D, Kanatani H, Yagi K, Hirabayashi K et al. Decrease in deoxyribonucleotide triphosphate pools and induction of alkaline-labile sites in mouse bone marrow cells by multiple treatments with methotrexate. Mutat Res 1993; 319: 143-149.
58. Pancheva SN. Methotrexate potentiates anti-herpes simplex virus type 1 activity of E-5-(2-bromovinyl)-20-deoxyuridine. Acta Virol 1995; 39: 117-119.
59. Yoshioka A, Tanaka S, Hiraoka O, Koyama Y, Hirota Y, Ayusawa D et al. Deoxyribonucleoside triphosphate imbalance. 5-Fluorodeoxyuridine-induced DNA double strand breaks in mouse FM3A cells and the mechanism of cell death. J Biol Chem 1987; 262: 8235-8241.
60. Yoshikawa R, Kusunoki M, Yanagi H, Noda M, Furuyama JI, Yamamura T et al. Dual antitumor effects of 5-fluorouracil on the cell cycle in colorectal carcinoma cells: a novel target mechanism concept for pharmacokinetic modulating chemotherapy. Cancer Res 2001; 61: 1029-1037.
61. Kawato Y, Aonuma M, Hirota Y, Kuga H, Sato K. Intracellular roles of SN-38, a metabolite of the camptothecin derivative CPT-11, in the antitumor effect of CPT-11. Cancer Res 1991; 51: 4187-4191.
62. Holm C, Covey JM, Kerrigan D, Pommier Y. Differential requirement of DNA replication for the cytotoxicity of DNA topoisomerase I and II inhibitors in Chinese hamster DC3F cells. Cancer Res 1989; 49: 6365-6368.
63. Amici C, Belardo G, Rossi A, Santoro MG. Activation of I kappa b kinase by herpes simplex virus type 1. A novel target for anti-herpetic therapy. J Biol Chem 2001; 276: 28759-28766.
64. Patel A, Hanson J, McLean TI, Olgiate J, Hilton M, Miller WE et al. Herpes simplex type 1 induction of persistent NF-kappa B nuclear translocation increases the efficiency of virus replication. Virology 1998; 247: 212-222.
65. Rong BL, Libermann TA, Kogawa K, Ghosh S, Cao LX, Pavan-Langston D et al. HSV-1-inducible proteins bind to NF-kappa B-like sites in the HSV-1 genome. Virology 1992; 189: 750-756.