Permissiveness of human cancer cells to oncolytic bovine herpesvirus 1 is mediated in part by KRAS activity

Journal of Virology

Volumn 88, Issue 12, 2014, Pages 6885-6895

  Cuddington, Breanne P ^a   Mossman, Karen L ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; ONCOLYTIC HERPES VIRUS;

ARTICLE; BOVINE HERPES VIRUS; CANCER CELL; CELL VIABILITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG DETERMINATION; DRUG EFFECT; DRUG TARGETING; EMBRYO; GENE MUTATION; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; NONHUMAN; ONCOGENE K RAS; PRIMARY CELL CULTURE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VIRAL TROPISM; VIRUS LOAD; VIRUS REPLICATION;

ANIMALS; CELL LINE, TUMOR; HUMANS; NEOPLASMS; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; PROTO-ONCOGENE PROTEINS; RAS PROTEINS; VIRUS REPLICATION;

EID: 84901366532     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00849-14     Document Type: Article

References (65)

1. Cervantes-Garcia D, Ortiz-Lopez R, Mayek-Perez N, Rojas-Martinez A. 2008. Oncolytic virotherapy. Ann. Hepatol. 7:34-45. http://www.medigraphic.com/pdfs/hepato/ah-2008/ah081e.pdf.
2. Vaha-Koskela MJ, Heikkila JE, Hinkkanen AE. 2007. Oncolytic viruses in cancer therapy. Cancer Lett. 254:178-216. http://dx.doi.org/10.1016/j.canlet.2007.02.002.
3. Russell SJ, Peng KW, Bell JC. 2012. Oncolytic virotherapy. Nat. Biotechnol. 30:658-670. http://dx.doi.org/10.1038/nbt.2287.
4. Shmulevitz M, Marcato P, Lee PW. 2005. Unshackling the links between reovirus oncolysis, Ras signaling, translational control and cancer. Oncogene 24:7720-7728. http://dx.doi.org/10.1038/sj.onc.1209041.
5. Martuza RL, Malick A, Markert JM, Ruffner KL, Coen DM. 1991. Experimental therapy of human glioma by means of a genetically engineered virus mutant. Science 252:854-856. http://dx.doi.org/10.1126/science.1851332.
6. Mossman KL, Saffran HA, Smiley JR. 2000. Herpes simplex virus ICP0 mutants are hypersensitive to interferon. J. Virol. 74:2052-2056. http://dx.doi.org/10.1128/JVI.74.4.2052-2056.2000.
7. Mossman KL, Smiley JR. 2002. Herpes simplex virus ICP0 and ICP34.5 counteract distinct interferon-induced barriers to virus replication. J. Virol. 76:1995-1998. http://dx.doi.org/10.1128/JVI.76.4.1995-1998.2002.
8. Everett RD, Boutell C, McNair C, Grant L, Orr A. 2010. Comparison of the biological and biochemical activities of several members of the alphaherpesvirus ICP0 family of proteins. J. Virol. 84:3476-3487. http://dx.doi.org/10.1128/JVI.02544-09.
9. Mossman KL, Smiley JR. 1999. Truncation of the C-terminal acidic transcriptional activation domain of herpes simplex virus VP16 renders expression of the immediate-early genes almost entirely dependent on ICP0. J. Virol. 73:9726-9733.
10. Hummel JL, Safroneeva E, Mossman KL. 2005. The role of ICP0-null HSV-1 and interferon signaling defects in the effective treatment of breast adenocarcinoma. Mol. Ther. 12:1101-1110. http://dx.doi.org/10.1016/j.ymthe.2005.07.533.
11. Workenhe ST, Pol JG, Lichty BD, Cummings DT, Mossman KL. Combining oncolytic HSV-1 with immunogenic cell death-inducing drug mitoxantrone breaks cancer immune tolerance and improves therapeutic efficacy. Cancer Immunol. Res. 5:1-11. http://dx.doi.org/10.1158/2326-6066.CIR-13-0059-T.
12. Sobol PT, Boudreau JE, Stephenson K, Wan Y, Lichty BD, Mossman KL. 2011. Adaptive antiviral immunity is a determinant of the therapeutic success of oncolytic virotherapy. Mol. Ther. 19:335-344. http://dx.doi.org/10.1038/mt.2010.264.
13. Workenhe ST, Simmons G, Pol JG, Lichty BD, Halford WP, Mossman KL. 2014. Immunogenic HSV mediated oncolysis shapes the antitumor immune response and contributes to therapeutic efficacy. Mol. Ther. 22: 123-131. http://dx.doi.org/10.1038/mt.2013.238.
14. Hushur O, Takashima Y, Matsumoto Y, Otsuka H. 2004. Restriction of bovine herpesvirus 1 (BHV-1) growth in non-permissive cells beyond the expression of immediate early genes. J. Vet. Med. Sci. 66:453-455. http://dx.doi.org/10.1292/jvms.66.453.
15. Turin L, Russo S, Poli G. 1999. BHV-1: new molecular approaches to control a common and widespread infection. Mol. Med. 5:261-284.
16. Jones C, Chowdhury S. 2007. A review of the biology of bovine herpesvirus type 1 (BHV-1), its role as a cofactor in the bovine respiratory disease complex and development of improved vaccines. Anim. Health Res. Rev. 8:187-205. http://dx.doi.org/10.1017/S146625230700134X.
17. Campadelli-Fiume G. 2000. Virus receptor arrays, CD46 and human herpesvirus 6. Trends Microbiol. 8:436-438. http://dx.doi.org/10.1016/S0966-842X(00)01804-7.
18. Merrill MK, Bernhardt G, Sampson JH, Wikstrand CJ, Bigner DD, Gromeier M. 2004. Poliovirus receptor CD155-targeted oncolysis of glioma. Neuro Oncol. 6:208-217. http://dx.doi.org/10.1215/S1152851703000577.
19. Pende D, Spaggiari GM, Marcenaro S, Martini S, Rivera P, Capobianco A, Falco M, Lanino E, Pierri I, Zambello R, Bacigalupo A, Mingari MC, Moretta A, Moretta L. 2005. Analysis of the receptor-ligand interactions in the natural killer-mediated lysis of freshly isolated myeloid or lymphoblastic leukemias: evidence for the involvement of the poliovirus receptor (CD155) and Nectin-2 (CD112). Blood 105:2066-2073. http://dx.doi.org/10.1182/blood-2004-09-3548.
20. Henderson G, Zhang Y, Jones C. 2005. The bovine herpesvirus 1 gene encoding infected cell protein 0 (bICP0) can inhibit interferon-dependent transcription in the absence of other viral genes. J. Gen. Virol. 86:2697-2702. http://dx.doi.org/10.1099/vir.0.81109-0.
21. Saira K, Zhou Y, Jones C. 2007. The infected cell protein 0 encoded by bovine herpesvirus 1 (bICP0) induces degradation of interferon response factor 3 and, consequently, inhibits beta interferon promoter activity. J. Virol. 81:3077-3086. http://dx.doi.org/10.1128/JVI.02064-06.
22. Rodrigues R, Cuddington B, Mossman K. 2010. Bovine herpesvirus type 1 as a novel oncolytic virus. Cancer Gene Ther. 17:344-355. http://dx.doi.org/10.1038/cgt.2009.77.
23. Cuddington BP, Dyer AL, Workenhe ST, Mossman KL. 2013. Oncolytic bovine herpesvirus type 1 infects and kills breast tumor cells and breast cancer-initiating cells irrespective of tumor subtype. Cancer Gene Ther. 20:282-289. http://dx.doi.org/10.1038/cgt.2013.18.
24. Ayllon V, Rebollo A. 2000. Ras-induced cellular events. Mol. Membr. Biol. 17:65-73. http://dx.doi.org/10.1080/09687680050117093.
25. Downward J. 2003. Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 3:11-22. http://dx.doi.org/10.1038/nrc969.
26. Rodriguez-Viciana P, Tetsu O, Oda K, Okada J, Rauen K, McCormick F. 2005. Cancer targets in the Ras pathway. Cold Spring Harb. Symp. Quant. Biol. 70:461-467. http://dx.doi.org/10.1101/sqb.2005.70.044.
27. Ferro E, Trabalzini L. 2010. RalGDS family members couple Ras to Ral signalling and that's not all. Cell. Signal. 22:1804-1810. http://dx.doi.org/10.1016/j.cellsig.2010.05.010.
28. Everts B, van der Poel HG. 2005. Replication-selective oncolytic viruses in the treatment of cancer. Cancer Gene Ther. 12:141-161. http://dx.doi.org/10.1038/sj.cgt.7700771.
29. Christian SL, Zu D, Licursi M, Komatsu Y, Pongnopparat T, Codner DA, Hirasawa K. 2012. Suppression of IFN-induced transcription underlies IFN defects generated by activated Ras/MEK in human cancer cells. PLoS One 7:e44267. http://dx.doi.org/10.1371/journal.pone.0044267.
30. Noser JA, Mael AA, Sakuma R, Ohmine S, Marcato P, Lee PW, Ikeda Y. 2007. The RAS/Raf1/MEK/ERK signaling pathway facilitates VSVmediated oncolysis: implication for the defective interferon response in cancer cells. Mol. Ther. 15:1531-1536. http://dx.doi.org/10.1038/sj.mt.6300193.
31. Battcock SM, Collier TW, Zu D, Hirasawa K. 2006. Negative regulation of the alpha interferon-induced antiviral response by the Ras/Raf/MEK pathway. J. Virol. 80:4422-4430. http://dx.doi.org/10.1128/JVI.80.9.4422-4430.2006.
32. Shmulevitz M, Pan LZ, Garant K, Pan D, Lee PW. 2010. Oncogenic Ras promotes reovirus spread by suppressing IFN-beta production through negative regulation of RIG-I signaling. Cancer Res. 70:4912-4921. http://dx.doi.org/10.1158/0008-5472.CAN-09-4676.
33. Wee S, Jagani Z, Xiang KX, Loo A, Dorsch M, Yao YM, Sellers WR, Lengauer C, Stegmeier F. 2009. PI3K pathway activation mediates resistance to MEK inhibitors in KRAS mutant cancers. Cancer Res. 69:4286-4293. http://dx.doi.org/10.1158/0008-5472.CAN-08-4765.
34. Bos JL. 1989. ras oncogenes in human cancer: a review. Cancer Res. 49:4682-4689.
35. Zhao S, Wang Y, Cao L, Ouellette MM, Freeman JW. 2010. Expression of oncogenic K-ras and loss of Smad4 cooperate to induce the expression of EGFR and to promote invasion of immortalized human pancreas ductal cells. Int. J. Cancer 127:2076-2087. http://dx.doi.org/10.1002/ijc.25412.
36. Leslie K, Gao SP, Berishaj M, Podsypanina K, Ho H, Ivashkiv L, Bromberg J. 2010. Differential interleukin-6/Stat3 signaling as a function of cellular context mediates Ras-induced transformation. Breast Cancer Res. 12:R80. http://dx.doi.org/10.1186/bcr2725.
37. Strong JE, Coffey MC, Tang D, Sabinin P, Lee PW. 1998. The molecular basis of viral oncolysis: usurpation of the Ras signaling pathway by reovirus. EMBO J. 17:3351-3362. http://dx.doi.org/10.1093/emboj/17.12.3351.
38. Davis JJ, Fang B. 2005. Oncolytic virotherapy for cancer treatment: challenges and solutions. J. Gene Med. 7:1380-1389. http://dx.doi.org/10.1002/jgm.800.
39. Farassati F, Yang AD, Lee PW. 2001. Oncogenes in Ras signalling pathway dictate host-cell permissiveness to herpes simplex virus 1. Nat. Cell Biol. 3:745-750. http://dx.doi.org/10.1038/35087061.
40. Norman KL, Hirasawa K, Yang AD, Shields MA, Lee PW. 2004. Reovirus oncolysis: the Ras/RalGEF/p38 pathway dictates host cell permissiveness to reovirus infection. Proc. Natl. Acad. Sci. U. S. A. 101:11099-11104. http://dx.doi.org/10.1073/pnas.0404310101.
41. Fraefel C, Zeng J, Choffat Y, Engels M, Schwyzer M, Ackermann M. 1994. Identification and zinc dependence of the bovine herpesvirus 1 transactivator protein BICP0. J. Virol. 68:3154-3162.
42. Saira K, Chowdhury S, Gaudreault N, da Silva L, Henderson G, Doster A, Jones C. 2008. The zinc RING finger of bovine herpesvirus 1-encoded bICP0 protein is crucial for viral replication and virulence. J. Virol. 82: 12060-12068. http://dx.doi.org/10.1128/JVI.01348-08.
43. Morgan TL, Yang DJ, Fry DG, Hurlin PJ, Kohler SK, Maher VM, McCormick JJ. 1991. Characteristics of an infinite life span diploid human fibroblast cell strain and a near-diploid strain arising from a clone of cells expressing a transfected v-myc oncogene. Exp. Cell Res. 197:125-136. http://dx.doi.org/10.1016/0014-4827(91)90489-H.
44. Geiser V, Zhang Y, Jones C. 2005. Analysis of a bovine herpesvirus 1 recombinant virus that does not express the bICP0 protein. J. Gen. Virol. 86:1987-1996. http://dx.doi.org/10.1099/vir.0.80921-0.
45. Workman A, Jones C. 2010. Productive infection and bICP0 early promoter activity of bovine herpesvirus 1 are stimulated by E2F1. J. Virol. 84:6308-6317. http://dx.doi.org/10.1128/JVI.00321-10.
46. Workman A, Jones C. 2011. Analysis of the cell cycle regulatory protein (E2F1) after infection of cultured cells with bovine herpesvirus 1 (BHV-1) or herpes simplex virus type 1 (HSV-1). Virus Res. 160:66-73. http://dx.doi.org/10.1016/j.virusres.2011.05.009.
47. Fan J, Bertino JR. 1997. K-ras modulates the cell cycle via both positive and negative regulatory pathways. Oncogene 14:2595-2607. http://dx.doi.org/10.1038/sj.onc.1201105.
48. Monticone M, Biollo E, Maffei M, Donadini A, Romeo F, Storlazzi CT, Giaretti W, Castagnola P. 2008. Gene expression deregulation by KRAS G12D and G12V in a BRAF V600E context. Mol. Cancer 7:92. http://dx.doi.org/10.1186/1476-4598-7-92.
49. Jia W, Zhou Q. 2005. Viral vectors for cancer gene therapy: viral dissemination and tumor targeting. Curr. Gene Ther. 5:133-142. http://dx.doi.org/10.2174/1566523052997460.
50. Shen Y, Nemunaitis J. 2006. Herpes simplex virus 1 (HSV-1) for cancer treatment. Cancer Gene Ther. 13:975-992. http://dx.doi.org/10.1038/sj.cgt.7700946.
51. Kaufman HL, Kim DW, DeRaffele G, Mitcham J, Coffin RS, Kim-Schulze S. 2010. 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. 17:718-730. http://dx.doi.org/10.1245/s10434-009-0809-6.
52. 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, Nemunaitis JJ. 2009. 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. 27:5763-5771. http://dx.doi.org/10.1200/JCO.2009.24.3675.
53. 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, Robertson T, Je JE, Lee YS, Parato K, Diallo JS, Fenster A, Daneshmand M, Bell JC, Kirn DH. 2011. Intravenous delivery of a multi-mechanistic cancer-targeted oncolytic poxvirus in humans. Nature 477:99-102. http://dx.doi.org/10.1038/nature10358.
54. Chen N, Bellone CJ, Schriewer J, Owens G, Fredrickson T, Parker S, Buller RM. 2011. Poxvirus interleukin-4 expression overcomes inherent resistance and vaccine-induced immunity: pathogenesis, prophylaxis, and antiviral therapy. Virology 409:328-337. http://dx.doi.org/10.1016/j.virol.2010.10.021.
55. Niller HH, Wolf H, Minarovits J. 2009. Epigenetic dysregulation of the host cell genome in Epstein-Barr virus-associated neoplasia. Semin. Cancer Biol. 19:158-164. http://dx.doi.org/10.1016/j.semcancer.2009.02.012.
56. Adhya D, Basu A. 2010. Epigenetic modulation of host: new insights into immune evasion by viruses. J. Biosci. 35:647-663. http://dx.doi.org/10.1007/s12038-010-0072-9.
57. Paschos K, Allday MJ. 2010. Epigenetic reprogramming of host genes in viral and microbial pathogenesis. Trends Microbiol. 18:439-447. http://dx.doi.org/10.1016/j.tim.2010.07.003.
58. Cullen BR. 2011. Viruses and microRNAs: RISCy interactions with serious consequences. Genes Dev. 25:1881-1894. http://dx.doi.org/10.1101/gad.17352611.
59. Lu F, Stedman W, Yousef M, Renne R, Lieberman PM. 2010. Epigenetic regulation of Kaposi's sarcoma-associated herpesvirus latency by virusencoded microRNAs that target Rta and the cellular Rbl2-DNMT pathway. J. Virol. 84:2697-2706. http://dx.doi.org/10.1128/JVI.01997-09.
60. DeGregori J, Kowalik T, Nevins JR. 1995. Cellular targets for activation by the E2F1 transcription factor include DNA synthesis-and G1/Sregulatory genes. Mol. Cell. Biol. 15:4215-4224.
61. Harbour JW, Dean DC. 2000. The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev. 14:2393-2409. http://dx.doi.org/10.1101/gad.813200.
62. Webb JD, Simon MC. 2010. Novel insights into the molecular origins and treatment of lung cancer. Cell Cycle 9:4098-4105. http://dx.doi.org/10.4161/cc.9.20.13588.
63. Okudela K, Woo T, Kitamura H. 2010. KRAS gene mutations in lung cancer: particulars established and issues unresolved. Pathol. Int. 60:651-660. http://dx.doi.org/10.1111/j.1440-1827.2010.02580.x.
64. Singh N, Bal A, Aggarwal AN, Das A, Behera D. 2010. Clinical outcomes in non-small-cell lung cancer in relation to expression of predictive and prognostic biomarkers. Future Oncol. 6:741-767. http://dx.doi.org/10.2217/fon.10.30.
65. Rossi A, Galetta D, Gridelli C. 2009. Biological prognostic and predictive factors in lung cancer. Oncology 77(Suppl 1):90-96. http://dx.doi.org/10.1159/000258500.