1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Cancer Biology
  4. Volume 2, 2018
  5. Article

Annual Review of Cancer Biology

Volume 2, 2018

Oncolytic Herpes Simplex Viruses as a Paradigm for the Treatment of Cancer

Abstract

Oncolytic viruses are native or modified viruses that directly kill tumor cells but spare normal tissue and promote host antitumor immunity. Recently, an oncolytic herpes simplex virus (oHSV) type 1–encoding human granulocyte-macrophage colony-stimulating factor (GM-CSF) demonstrated significant clinical benefit in a randomized phase III clinical trial for patients with advanced melanoma, leading to regulatory approval in 2015. In this review, we provide a general characterization of herpes simplex viruses and discuss methods for vector modification, which can help limit viral pathogenicity and immunogenicity while promoting antitumor immunogenicity. We also provide insight into general strategies for using oHSV agents in tumor immunotherapy regimens for the treatment of cancer and briefly review some of the currently emerging preclinical and clinical data that support an important role for such agents in the treatment of cancer.

Keyword(s): HSV, immuno-virotherapy, immunotherapy, melanoma, oncolytic viruses, T-VEC
Loading

Article metrics loading...

/content/journals/10.1146/annurev-cancerbio-030617-050254
2018-03-04
2025-04-27
Loading full text...

Full text loading...

/deliver/fulltext/cancerbio/2/1/annurev-cancerbio-030617-050254.html?itemId=/content/journals/10.1146/annurev-cancerbio-030617-050254&mimeType=html&fmt=ahah

Literature Cited

  1. Advani SJ, Markert JM, Sood RF, Samuel S, Gillespie GY. et al. 2011. Increased oncolytic efficacy for high-grade gliomas by optimal integration of ionizing radiation into the replicative cycle of HSV-1. Gene Ther 18:1098–102 [Google Scholar]
  2. Aghi M, Rabkin S, Martuza RL. 2006. Effect of chemotherapy-induced DNA repair on oncolytic herpes simplex viral replication. J. Natl. Cancer Inst. 98:38–50 [Google Scholar]
  3. Aghi M, Visted T, Depinho RA, Chiocca EA. 2008. Oncolytic herpes virus with defective ICP6 specifically replicates in quiescent cells with homozygous genetic mutations in p16. Oncogene 27:4249–54 [Google Scholar]
  4. Ahmad A, Sharif-Askari E, Fawaz L, Menezes J. 2000. Innate immune response of the human host to exposure with herpes simplex virus type 1: in vitro control of the virus infection by enhanced natural killer activity via interleukin-15 induction. J. Virol. 74:7196–203 [Google Scholar]
  5. Ahn K, Meyer TH, Uebel S, Sempe P, Djaballah H. et al. 1996. Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus ICP47. EMBO J 15:3247–55 [Google Scholar]
  6. Akhtar J, Shukla D. 2009. Viral entry mechanisms: cellular and viral mediators of herpes simplex virus entry. FEBS J 276:7228–36 [Google Scholar]
  7. Alvarez-Breckenridge CA, Yu J, Price R, Wojton J, Pradarelli J. et al. 2012. NK cells impede glioblastoma virotherapy through NKp30 and NKp46 natural cytotoxicity receptors. Nat. Med. 18:1827–34 [Google Scholar]
  8. Andtbacka RH, Agarwala SS, Ollila DW, Hallmeyer S, Milhem M. et al. 2016. Cutaneous head and neck melanoma in OPTiM, a randomized phase 3 trial of talimogene laherparepvec versus granulocyte-macrophage colony-stimulating factor for the treatment of unresected stage IIIB/IIIC/IV melanoma. Head Neck 38:1752–58 [Google Scholar]
  9. Andtbacka RH, Kaufman HL, Collichio F, Amatruda T, Senzer N. et al. 2015. Talimogene laherparepvec improves durable response rate in patients with advanced melanoma. J. Clin. Oncol. 33:2780–88 [Google Scholar]
  10. Aubert M, Blaho JA. 1999. The herpes simplex virus type 1 regulatory protein ICP27 is required for the prevention of apoptosis in infected human cells. J. Virol. 73:2803–13 [Google Scholar]
  11. Baringer JR. 2008. Herpes simplex infections of the nervous system. Neurol. Clin. 26:657–74 [Google Scholar]
  12. Bedoui S, Greyer M. 2014. The role of dendritic cells in immunity against primary herpes simplex virus infections. Front. Microbiol. 5:533 [Google Scholar]
  13. Bennett JJ, Tjuvajev J, Johnson P, Doubrovin M, Akhurst T. et al. 2001. Positron emission tomography imaging for herpes virus infection: implications for oncolytic viral treatments of cancer. Nat. Med. 7:859–63 [Google Scholar]
  14. Bi Y, Sun L, Gao D, Ding C, Li Z. et al. 2014. High-efficiency targeted editing of large viral genomes by RNA-guided nucleases. PLOS Pathog 10:e1004090 [Google Scholar]
  15. Bloom DC. 2016. Alphaherpesvirus latency: a dynamic state of transcription and reactivation. Adv. Virus. Res. 94:53–80 [Google Scholar]
  16. Bolyard C, Meisen WH, Banasavadi-Siddegowda Y, Hardcastle J, Yoo JY. et al. 2017. BAI1 orchestrates macrophage inflammatory response to HSV infection—implications for oncolytic viral therapy. Clin. Cancer Res. 23:1809–19 [Google Scholar]
  17. Bommareddy PK, Patel A, Hossain S, Kaufman HL. 2017.a Talimogene laherparepvec (T-VEC) and other oncolytic viruses for the treatment of melanoma. Am. J. Clin. Dermatol. 18:1–15 [Google Scholar]
  18. Bommareddy PK, Silk AW, Kaufman HL. 2017.b Intratumoral approaches for the treatment of melanoma. Cancer J 23:40–47 [Google Scholar]
  19. Boutell C, Everett RD. 2013. Regulation of alphaherpesvirus infections by the ICP0 family of proteins. J Gen. Virol. 94:465–81 [Google Scholar]
  20. Bradley H, Markowitz LE, Gibson T, McQuillan GM. 2014. Seroprevalence of herpes simplex virus types 1 and 2—United States, 1999–2010. J. Infect. Dis. 209:325–33 [Google Scholar]
  21. Campadelli-Fiume G, Menotti L, Avitabile E, Gianni T. 2012. Viral and cellular contributions to herpes simplex virus entry into the cell. Curr. Opin. Virol. 2:28–36 [Google Scholar]
  22. Campadelli-Fiume G, Petrovic B, Leoni V, Gianni T, Avitabile E. et al. 2016. Retargeting strategies for oncolytic herpes simplex viruses. Viruses 8:63 [Google Scholar]
  23. Cassady KA, Gross M, Gillespie GY, Roizman B. 2002. Second-site mutation outside of the US10-12 domain of Δγ134.5 herpes simplex virus 1 recombinant blocks the shutoff of protein synthesis induced by activated protein kinase R and partially restores neurovirulence. J. Virol. 76:942–49 [Google Scholar]
  24. Cassady KA, Gross M, Roizman B. 1998. The herpes simplex virus US11 protein effectively compensates for the γ134.5 gene if present before activation of protein kinase R by precluding its phosphorylation and that of the α subunit of eukaryotic translation initiation factor 2. J. Virol. 72:8620–26 [Google Scholar]
  25. Cheema TA, Kanai R, Kim GW, Wakimoto H, Passer B. et al. 2011. Enhanced antitumor efficacy of low-dose etoposide with oncolytic herpes simplex virus in human glioblastoma stem cell xenografts. Clin. Cancer Res. 17:7383–93 [Google Scholar]
  26. Cheema TA, Wakimoto H, Fecci PE, Ning J, Kuroda T. et al. 2013. Multifaceted oncolytic virus therapy for glioblastoma in an immunocompetent cancer stem cell model. PNAS 110:12006–11 [Google Scholar]
  27. Chen X, Han J, Chu J, Zhang L, Zhang J. et al. 2016. A combinational therapy of EGFR-CAR NK cells and oncolytic herpes simplex virus 1 for breast cancer brain metastases. Oncotarget 7:27764–77 [Google Scholar]
  28. Cheng G, Feng Z, HE B. 2005. Herpes simplex virus 1 infection activates the endoplasmic reticulum resident kinase PERK and mediates eIF-2α dephosphorylation by the γ134.5 protein. J. Virol. 79:1379–88 [Google Scholar]
  29. Chew T, Taylor KE, Mossman KL. 2009. Innate and adaptive immune responses to herpes simplex virus. Viruses 1:979–1002 [Google Scholar]
  30. Chou J, Kern ER, Whitley RJ, Roizman B. 1990. Mapping of herpes simplex virus-1 neurovirulence to gamma 134.5, a gene nonessential for growth in culture. Science 250:1262–66 [Google Scholar]
  31. Christensen MH, Jensen SB, Miettinen JJ, Luecke S, Prabakaran T. et al. 2016. HSV-1 ICP27 targets the TBK1-activated STING signalsome to inhibit virus-induced type I IFN expression. EMBO J 35:1385–99 [Google Scholar]
  32. Deluca NA, Schaffer PA. 1985. Activation of immediate-early, early, and late promoters by temperature-sensitive and wild-type forms of herpes simplex virus type 1 protein ICP4. Mol. Cell Biol. 5:1997–2008 [Google Scholar]
  33. Deschamps T, Kalamvoki M. 2017. Impaired STING pathway in the human osteosarcoma U2OS cells contributes to the growth of ICP0-null mutant herpes simplex virus. J. Virol. 91:e00006–17 [Google Scholar]
  34. Diner BA, Lum KK, Javitt A, Cristea IM. 2015. Interactions of the antiviral factor interferon gamma-inducible protein 16 (IFI16) mediate immune signaling and herpes simplex virus-1 immunosuppression. Mol. Cell Proteom. 14:2341–56 [Google Scholar]
  35. Dufour F, Sasseville AM, Chabaud S, Massie B, Siegel RM, Langelier Y. 2011. The ribonucleotide reductase R1 subunits of herpes simplex virus types 1 and 2 protect cells against TNFα- and FasL-induced apoptosis by interacting with caspase-8. Apoptosis 16:256–71 [Google Scholar]
  36. Egan KP, Wu S, Wigdahl B, Jennings SR. 2013. Immunological control of herpes simplex virus infections. J. Neurovirol. 19:328–45 [Google Scholar]
  37. Eggensperger S, Tampe R. 2015. The transporter associated with antigen processing: a key player in adaptive immunity. Biol. Chem. 396:1059–72 [Google Scholar]
  38. Ellermann-Eriksen S. 2005. Macrophages and cytokines in the early defence against herpes simplex virus. Virol. J. 2:59 [Google Scholar]
  39. Everett RD. 2015. Dynamic response of IFI16 and promyelocytic leukemia nuclear body components to herpes simplex virus 1 infection. J. Virol. 90:167–79 [Google Scholar]
  40. Fujioka N, Akazawa R, Ohashi K, Fujii M, Ikeda M, Kurimoto M. 1999. Interleukin-18 protects mice against acute herpes simplex virus type 1 infection. J. Virol. 73:2401–9 [Google Scholar]
  41. Fulci G, Dmitrieva N, Gianni D, Fontana EJ, Pan X. et al. 2007. Depletion of peripheral macrophages and brain microglia increases brain tumor titers of oncolytic viruses. Cancer Res 67:9398–406 [Google Scholar]
  42. Gatta V, Petrovic B, Campadelli-Fiume G. 2015. The engineering of a novel ligand in gH confers to HSV an expanded tropism independent of gD activation by its receptors. PLOS Pathog 11:e1004907 [Google Scholar]
  43. Gobeil PA, Leib DA. 2012. Herpes simplex virus γ34.5 interferes with autophagosome maturation and antigen presentation in dendritic cells. mBio 3:e00267–12 [Google Scholar]
  44. Goins WF, Hall B, Cohen JB, Glorioso JC. 2016. Retargeting of herpes simplex virus (HSV) vectors. Curr. Opin. Virol. 21:93–101 [Google Scholar]
  45. Grandi P, Fernandez J, Szentirmai O, Carter R, Gianni D. et al. 2010. Targeting HSV-1 virions for specific binding to epidermal growth factor receptor-vIII-bearing tumor cells. Cancer Gene Ther 17:655–63 [Google Scholar]
  46. Grauwet K, Cantoni C, Parodi M, De Maria A Devriendt B. et al. 2014. Modulation of CD112 by the alphaherpesvirus gD protein suppresses DNAM-1-dependent NK cell-mediated lysis of infected cells. PNAS 111:16118–23 [Google Scholar]
  47. Guo H, Omoto S, Harris PA, Finger JN, Bertin J. et al. 2015. Herpes simplex virus suppresses necroptosis in human cells. Cell Host Microbe 17:243–51 [Google Scholar]
  48. Han J, Chen X, Chu J, Xu B, Meisen WH. et al. 2015. TGFβ treatment enhances glioblastoma virotherapy by inhibiting the innate immune response. Cancer Res 75:5273–82 [Google Scholar]
  49. Hardcastle J, Kurozumi K, Dmitrieva N, Sayers MP, Ahmad S. et al. 2010. Enhanced antitumor efficacy of vasculostatin (Vstat120) expressing oncolytic HSV-1. Mol. Ther. 18:285–94 [Google Scholar]
  50. Harle P, Sainz B Jr., Carr DJ, Halford WP. 2002. The immediate-early protein, ICP0, is essential for the resistance of herpes simplex virus to interferon-α/β. Virology 293:295–304 [Google Scholar]
  51. He B, Gross M, Roizman B. 1997. The γ134.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1α to dephosphorylate the α subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNA-activated protein kinase. PNAS 94:843–48 [Google Scholar]
  52. Heilingloh CS, Muhl-Zurbes P, Steinkasserer A, Kummer M. 2014. Herpes simplex virus type 1 ICP0 induces CD83 degradation in mature dendritic cells independent of its E3 ubiquitin ligase function. J. Gen. Virol. 95:1366–75 [Google Scholar]
  53. Hook LM, Friedman HM. 2007. Subversion of innate and adaptive immunity: immune evasion from antibody and complement. Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis A Arvin, G Campadelli-Fiume, E Mocarski, PS Moore, B Roizman et al. Cambridge, UK: Cambridge Univ. Press https://www.ncbi.nlm.nih.gov/books/NBK47412/ [Google Scholar]
  54. Hook LM, Lubinski JM, Jiang M, Pangburn MK, Friedman HM. 2006. Herpes simplex virus type 1 and 2 glycoprotein C prevents complement-mediated neutralization induced by natural immunoglobulin M antibody. J. Virol. 80:4038–46 [Google Scholar]
  55. Hu JCC, Coffin RS, Davis CJ, Graham NJ, Groves N. et al. 2006. A phase I study of OncoVEXGM-CSF, a second-generation oncolytic herpes simplex virus expressing granulocyte macrophage colony-stimulating factor. Clin. Cancer Res. 12:6737–47 [Google Scholar]
  56. 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. 12:1101–10 [Google Scholar]
  57. Ikeda K, Ichikawa T, Wakimoto H, Silver JS, Deisboeck TS. et al. 1999. Oncolytic virus therapy of multiple tumors in the brain requires suppression of innate and elicited antiviral responses. Nat. Med. 5:881–87 [Google Scholar]
  58. Ikeda K, Wakimoto H, Ichikawa T, Jhung S, Hochberg FH. et al. 2000. Complement depletion facilitates the infection of multiple brain tumors by an intravascular, replication-conditional herpes simplex virus mutant. J. Virol. 74:4765–75 [Google Scholar]
  59. Imai T, Koyanagi N, Ogawa R, Shindo K, Suenaga T. et al. 2013. Us3 kinase encoded by herpes simplex virus 1 mediates downregulation of cell surface major histocompatibility complex class I and evasion of CD8+ T cells. PLOS ONE 8:e72050 [Google Scholar]
  60. Jacobs A, Tjuvajev JG, Dubrovin M, Akhurst T, Balatoni J. et al. 2001. Positron emission tomography-based imaging of transgene expression mediated by replication-conditional, oncolytic herpes simplex virus type 1 mutant vectors in vivo. Cancer Res 61:2983–95 [Google Scholar]
  61. Jerome KR, Chen Z, Lang R, Torres MR, Hofmeister J. et al. 2001. HSV and glycoprotein J inhibit caspase activation and apoptosis induced by granzyme B or Fas. J. Immunol. 167:3928–35 [Google Scholar]
  62. Jhawar SR, Thandoni A, Bommareddy PK, Hassan S, Kohlhapp FJ. et al. 2017. Oncolytic viruses—natural and genetically engineered cancer immunotherapies. Front. Oncol. 7:202 [Google Scholar]
  63. Jin H, Ma Y, Prabhakar BS, Feng Z, Valyi-Nagy T. et al. 2009. The γ134.5 protein of herpes simplex virus 1 is required to interfere with dendritic cell maturation during productive infection. J. Virol. 83:4984–94 [Google Scholar]
  64. Johnson KE, Song B, Knipe DM. 2008. Role for herpes simplex virus 1 ICP27 in the inhibition of type I interferon signaling. Virology 374:487–94 [Google Scholar]
  65. Kalamvoki M, Roizman B. 2014. HSV-1 degrades, stabilizes, requires, or is stung by STING depending on ICP0, the US3 protein kinase, and cell derivation. PNAS 111:E611–17 [Google Scholar]
  66. Kanai R, Rabkin SD. 2013. Combinatorial strategies for oncolytic herpes simplex virus therapy of brain tumors. CNS Oncol 2:129–42 [Google Scholar]
  67. Kanai R, Rabkin SD, Yip S, Sgubin D, Zaupa CM. et al. 2012. Oncolytic virus-mediated manipulation of DNA damage responses: synergy with chemotherapy in killing glioblastoma stem cells. J. Natl. Cancer Inst. 104:42–55 [Google Scholar]
  68. Kanai R, Wakimoto H, Martuza RL, Rabkin SD. 2011. A novel oncolytic herpes simplex virus that synergizes with phosphoinositide 3-kinase/Akt pathway inhibitors to target glioblastoma stem cells. Clin. Cancer Res. 17:3686–96 [Google Scholar]
  69. 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. 17:718–30 [Google Scholar]
  70. Kaufman HL, Kohlhapp FJ, Zloza A. 2015. Oncolytic viruses: a new class of immunotherapy drugs. Nat. Rev. Drug Discov. 14:642–62 [Google Scholar]
  71. Kaur B, Chiocca EA, Cripe TP. 2012. Oncolytic HSV-1 virotherapy: clinical experience and opportunities for progress. Curr. Pharm. Biotechnol. 13:1842–51 [Google Scholar]
  72. Kelly E, Russell SJ. 2007. History of oncolytic viruses: genesis to genetic engineering. Mol. Ther. 15:651–59 [Google Scholar]
  73. Kuroda T, Rabkin SD, Martuza RL. 2006. Effective treatment of tumors with strong β-catenin/T-cell factor activity by transcriptionally targeted oncolytic herpes simplex virus vector. Cancer Res 66:10127–35 [Google Scholar]
  74. Lawler SE, Speranza MC, Cho CF, Chiocca EA. 2017. Oncolytic viruses in cancer treatment: a review. JAMA Oncol 3:841–49 [Google Scholar]
  75. Lee CY, Rennie PS, Jia WW. 2009. MicroRNA regulation of oncolytic herpes simplex virus-1 for selective killing of prostate cancer cells. Clin. Cancer Res. 15:5126–35 [Google Scholar]
  76. Leoni V, Gianni T, Salvioli S, Campadelli-Fiume G. 2012. Herpes simplex virus glycoproteins gH/gL and gB bind Toll-like receptor 2, and soluble gH/gL is sufficient to activate NF-κB. J. Virol. 86:6555–62 [Google Scholar]
  77. Leske H, Haase R, Restle F, Schichor C, Albrecht V. et al. 2012. Varicella zoster virus infection of malignant glioma cell cultures: a new candidate for oncolytic virotherapy. Anticancer Res 32:1137–44 [Google Scholar]
  78. Lin C, Li H, Hao M, Xiong D, Luo Y. et al. 2016. Increasing the efficiency of CRISPR/Cas9-mediated precise genome editing of HSV-1 virus in human cells. Sci. Rep. 6:34531 [Google Scholar]
  79. Lin R, Noyce RS, Collins SE, Everett RD, Mossman KL. 2004. The herpes simplex virus ICP0 RING finger domain inhibits IRF3- and IRF7-mediated activation of interferon-stimulated genes. J. Virol. 78:1675–84 [Google Scholar]
  80. Liu BL, Robinson M, Han ZQ, Branston RH, English C. et al. 2003. ICP34.5 deleted herpes simplex virus with enhanced oncolytic, immune stimulating, and anti-tumour properties. Gene. Ther. 10:292–303 [Google Scholar]
  81. Liu J, Gallo RM, Duffy C, Brutkiewicz RR. 2016. A VP22-null HSV-1 is impaired in inhibiting CD1d-mediated antigen presentation. Viral. Immunol. 29:409–16 [Google Scholar]
  82. Liu Y, Lin R, Olagnier D. 2017. RIGulation of STING expression: at the crossroads of viral RNA and DNA sensing pathways. Inflamm. Cell Signal. 4:e1491 [Google Scholar]
  83. Looker KJ, Magaret AS, May MT, Turner KM, Vickerman P. et al. 2015. Global and regional estimates of prevalent and incident herpes simplex virus type 1 infections in 2012. PLOS ONE 10:e0140765 [Google Scholar]
  84. Lubinski J, Nagashunmugam T, Friedman HM. 1998. Viral interference with antibody and complement. Semin. Cell Dev. Biol. 9:329–37 [Google Scholar]
  85. Luecke S, Paludan SR. 2015. Innate recognition of alphaherpesvirus DNA. Adv. Virus Res. 92:63–100 [Google Scholar]
  86. Luo C, Mori I, Goshima F, Ushijima Y, Nawa A. et al. 2007. Replication-competent, oncolytic herpes simplex virus type 1 mutants induce a bystander effect following ganciclovir treatment. J. Gene. Med. 9:875–83 [Google Scholar]
  87. Ma Y, Jin H, Valyi-Nagy T, Cao Y, Yan Z, He B. 2012. Inhibition of TANK binding kinase 1 by herpes simplex virus 1 facilitates productive infection. J. Virol. 86:2188–96 [Google Scholar]
  88. 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 252:854–56 [Google Scholar]
  89. Mazzacurati L, Marzulli M, Reinhart B, Miyagawa Y, Uchida H. et al. 2015. Use of miRNA response sequences to block off-target replication and increase the safety of an unattenuated, glioblastoma-targeted oncolytic HSV. Mol. Ther. 23:99–107 [Google Scholar]
  90. McKie EA, Maclean AR, Lewis AD, Cruickshank G, Rampling R. et al. 1996. Selective in vitro replication of herpes simplex virus type 1 (HSV-1) ICP34.5 null mutants in primary human CNS tumours—evaluation of a potentially effective clinical therapy. Br. J. Cancer 74:745–52 [Google Scholar]
  91. Meisen WH, Wohleb ES, Jaime-Ramirez AC, Bolyard C, Yoo JY. et al. 2015. The impact of macrophage- and microglia-secreted TNFα on oncolytic HSV-1 therapy in the glioblastoma tumor microenvironment. Clin. Cancer Res. 21:3274–85 [Google Scholar]
  92. Melchjorsen J, Matikainen S, Paludan SR. 2009. Activation and evasion of innate antiviral immunity by herpes simplex virus. Viruses 1:737–59 [Google Scholar]
  93. Melchjorsen J, Siren J, Julkunen I, Paludan SR, Matikainen S. 2006. Induction of cytokine expression by herpes simplex virus in human monocyte-derived macrophages and dendritic cells is dependent on virus replication and is counteracted by ICP27 targeting NF-κ;B and IRF-3. J. Gen. Virol. 87:1099–108 [Google Scholar]
  94. Mineta T, Rabkin SD, Martuza RL. 1994. Treatment of malignant gliomas using ganciclovir-hypersensitive, ribonucleotide reductase-deficient herpes simplex viral mutant. Cancer Res 54:3963–66 [Google Scholar]
  95. Mittnacht S, Straub P, Kirchner H, Jacobsen H. 1988. Interferon treatment inhibits onset of herpes simplex virus immediate-early transcription. Virology 164:201–10 [Google Scholar]
  96. Miyatake S, Iyer A, Martuza RL, Rabkin SD. 1997. Transcriptional targeting of herpes simplex virus for cell-specific replication. J. Virol. 71:5124–32 [Google Scholar]
  97. Mohr I, Gluzman Y. 1996. A herpesvirus genetic element which affects translation in the absence of the viral GADD34 function. EMBO J 15:4759–66 [Google Scholar]
  98. Momburg F, Hengel H. 2002. Corking the bottleneck: the transporter associated with antigen processing as a target for immune subversion by viruses. Curr. Top. Microbiol. Immunol. 269:57–74 [Google Scholar]
  99. Murphy JA, Duerst RJ, Smith TJ, Morrison LA. 2003. Herpes simplex virus type 2 virion host shutoff protein regulates alpha/beta interferon but not adaptive immune responses during primary infection in vivo. J. Virol. 77:9337–45 [Google Scholar]
  100. Nagel CH, Pohlmann A, Sodeik B. 2014. Construction and characterization of bacterial artificial chromosomes (BACs) containing herpes simplex virus full-length genomes. Methods Mol. Biol. 1144:43–62 [Google Scholar]
  101. Nakashima H, Chiocca EA. 2014. Modification of HSV-1 to an oncolytic virus. Methods Mol. Biol. 1144:117–27 [Google Scholar]
  102. Nanda D, Vogels R, Havenga M, Avezaat CJ, Bout A, Smitt PS. 2001. Treatment of malignant gliomas with a replicating adenoviral vector expressing herpes simplex virus-thymidine kinase. Cancer Res 61:8743–50 [Google Scholar]
  103. Neumann J, Eis-Hubinger AM, Koch N. 2003. Herpes simplex virus type 1 targets the MHC class II processing pathway for immune evasion. J. Immunol. 171:3075–83 [Google Scholar]
  104. Niazy N, Temme S, Bocuk D, Giesen C, Konig A. et al. 2017. Misdirection of endosomal trafficking mediated by herpes simplex virus-encoded glycoprotein B. FASEB J 31:1650–67 [Google Scholar]
  105. Ning J, Wakimoto H. 2014. Oncolytic herpes simplex virus-based strategies: toward a breakthrough in glioblastoma therapy. Front. Microbiol. 5:303 [Google Scholar]
  106. Ning J, Wakimoto H, Peters C, Martuza RL, Rabkin SD. 2017. Rad51 degradation: role in oncolytic virus-poly(ADP-ribose) polymerase inhibitor combination therapy in glioblastoma. J. Natl. Cancer Inst. 109:1–13 [Google Scholar]
  107. Oberman F, Panet A. 1988. Inhibition of transcription of herpes simplex virus immediate early genes in interferon-treated human cells. J. Gen. Virol. 69:1167–77 [Google Scholar]
  108. Paludan SR, Bowie AG, Horan KA, Fitzgerald KA. 2011. Recognition of herpesviruses by the innate immune system. Nat. Rev. Immunol. 11:143–54 [Google Scholar]
  109. Parker JN, Gillespie GY, Love CE, Randall S, Whitley RJ, Markert JM. 2000. Engineered herpes simplex virus expressing IL-12 in the treatment of experimental murine brain tumors. PNAS 97:2208–13 [Google Scholar]
  110. Passer BJ, Cheema T, Wu S, Wu CL, Rabkin SD, Martuza RL. 2013. Combination of vinblastine and oncolytic herpes simplex virus vector expressing IL-12 therapy increases antitumor and antiangiogenic effects in prostate cancer models. Cancer Gene. Ther. 20:17–24 [Google Scholar]
  111. Pellett PE, Roizman B. 2013. Herpesviridae. Fields Virology DM Knipe, P Howley, pp. 1802–22 Philadelphia: Lippincott Williams & Wilkins, 6th ed.. [Google Scholar]
  112. Peters C, Rabkin SD. 2015. Designing herpes viruses as oncolytics. Mol. Ther. Oncolytics 2:15010 [Google Scholar]
  113. Petrovic B, Gianni T, Gatta V, Campadelli-Fiume G. 2017. Insertion of a ligand to HER2 in gB retargets HSV tropism and obviates the need for activation of the other entry glycoproteins. PLOS Pathog 13:e1006352 [Google Scholar]
  114. Pollara G, Speidel K, Samady L, Rajpopat M, McGrath Y. et al. 2003. Herpes simplex virus infection of dendritic cells: balance among activation, inhibition, and immunity. J. Infect. Dis. 187:165–78 [Google Scholar]
  115. Poppers J, Mulvey M, Khoo D, Mohr I. 2000. Inhibition of PKR activation by the proline-rich RNA binding domain of the herpes simplex virus type 1 Us11 protein. J. Virol. 74:11215–21 [Google Scholar]
  116. Pourchet A, Fuhrmann SR, Pilones KA, Demaria S, Frey AB. et al. 2016. CD8+ T-cell immune evasion enables oncolytic virus immunotherapy. EBioMedicine 5:59–67 [Google Scholar]
  117. Puzanov I, Milhem MM, Minor D, Hamid O, Li A. et al. 2016. Talimogene laherparepvec in combination with ipilimumab in previously untreated, unresectable stage IIIB-IV melanoma. J. Clin. Oncol. 34:2619–26 [Google Scholar]
  118. Rao P, Pham HT, Kulkarni A, Yang Y, Liu X. et al. 2011. Herpes simplex virus 1 glycoprotein B and US3 collaborate to inhibit CD1d antigen presentation and NKT cell function. J. Virol. 85:8093–104 [Google Scholar]
  119. Rasmussen SB, Sorensen LN, Malmgaard L, Ank N, Baines JD. et al. 2007. Type I interferon production during herpes simplex virus infection is controlled by cell-type-specific viral recognition through Toll-like receptor 9, the mitochondrial antiviral signaling protein pathway, and novel recognition systems. J. Virol. 81:13315–24 [Google Scholar]
  120. Ribas A, Dummer R, Puzanov I, VanderWalde A, Andtbacka RHI. et al. 2017. Oncolytic virotherapy promotes intratumoral T cell infiltration and improves anti-PD-1 immunotherapy. Cell 170:1109–19 [Google Scholar]
  121. Roizman B, Jenkins FJ. 1985. Genetic engineering of novel genomes of large DNA viruses. Science 229:1208–14 [Google Scholar]
  122. Roizman B, Knipe DM, Whitley RJ. 2013. Herpes simplex viruses. Fields Virology DM Knipe, P Howley 1823–97 Philadelphia: Lippincott Williams & Wilkins, 6th ed.. [Google Scholar]
  123. Russell TA, Stefanovic T, Tscharke DC. 2015. Engineering herpes simplex viruses by infection–transfection methods including recombination site targeting by CRISPR/Cas9 nucleases. J. Virol. Methods 213:18–25 [Google Scholar]
  124. Saha D, Ahmed SS, Rabkin SD. 2015. Exploring the antitumor effect of virus in malignant glioma. Drugs Future 40:739–49 [Google Scholar]
  125. Saha D, Wakimoto H, Rabkin SD. 2016. Oncolytic herpes simplex virus interactions with the host immune system. Curr. Opin. Virol. 21:26–34 [Google Scholar]
  126. Sanchez R, Mohr I. 2007. Inhibition of cellular 2′-5′ oligoadenylate synthetase by the herpes simplex virus type 1 Us11 protein. J. Virol. 81:3455–64 [Google Scholar]
  127. Sato A, Linehan MM, Iwasaki A. 2006. Dual recognition of herpes simplex viruses by TLR2 and TLR9 in dendritic cells. PNAS 103:17343–48 [Google Scholar]
  128. Sen J, Liu X, Roller R, Knipe DM. 2013. Herpes simplex virus US3 tegument protein inhibits Toll-like receptor 2 signaling at or before TRAF6 ubiquitination. Virology 439:65–73 [Google Scholar]
  129. Senzer NN, Kaufman HL, Amatruda T, Nemunaitis M, Reid T. et al. 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. 27:5763–71 [Google Scholar]
  130. Shen G, Wang K, Wang S, Cai M, Li ML, Zheng C. 2014. Herpes simplex virus 1 counteracts viperin via its virion host shutoff protein UL41. J. Virol. 88:12163–66 [Google Scholar]
  131. Sievers E, Neumann J, Raftery M, Schonrich G, Eis-Hubinger AM, Koch N. 2002. Glycoprotein B from strain 17 of herpes simplex virus type I contains an invariant chain homologous sequence that binds to MHC class II molecules. Immunology 107:129–35 [Google Scholar]
  132. Sobol PT, Hummel JL, Rodrigues RM, Mossman KL. 2009. PML has a predictive role in tumor cell permissiveness to interferon-sensitive oncolytic viruses. Gene. Ther. 16:1077–87 [Google Scholar]
  133. Sobol PT, Mossman KL. 2006. ICP0 prevents RNase L-independent rRNA cleavage in herpes simplex virus type 1-infected cells. J. Virol. 80:218–25 [Google Scholar]
  134. Su C, Zhan G, Zheng C. 2016. Evasion of host antiviral innate immunity by HSV-1, an update. Virol. J. 13:38 [Google Scholar]
  135. Su C, Zhang J, Zheng C. 2015. Herpes simplex virus 1 UL41 protein abrogates the antiviral activity of hZAP by degrading its mRNA. Virol. J. 12:203 [Google Scholar]
  136. Suazo PA, Ibanez FJ, Retamal-Diaz AR, Paz-Fiblas MV, Bueno SM. et al. 2015. Evasion of early antiviral responses by herpes simplex viruses. Mediat. Inflamm. 2015:593757 [Google Scholar]
  137. Suenaga T, Kohyama M, Hirayasu K, Arase H. 2014. Engineering large viral DNA genomes using the CRISPR-Cas9 system. Microbiol. Immunol. 58:513–22 [Google Scholar]
  138. Sundaresan P, Hunter WD, Martuza RL, Rabkin SD. 2000. Attenuated, replication-competent herpes simplex virus type 1 mutant G207: safety evaluation in mice. J. Virol. 74:3832–41 [Google Scholar]
  139. Takakuwa H, Goshima F, Nozawa N, Yoshikawa T, Kimata H. et al. 2003. Oncolytic viral therapy using a spontaneously generated herpes simplex virus type 1 variant for disseminated peritoneal tumor in immunocompetent mice. Arch. Virol. 148:813–25 [Google Scholar]
  140. Temme S, Eis-Hubinger AM, McLellan AD, Koch N. 2010. The herpes simplex virus-1 encoded glycoprotein B diverts HLA-DR into the exosome pathway. J. Immunol. 184:236–43 [Google Scholar]
  141. Tischer BK, Kaufer BB. 2012. Viral bacterial artificial chromosomes: generation, mutagenesis, and removal of mini-F sequences. J. Biomed. Biotechnol. 2012:472537 [Google Scholar]
  142. Todo T, Martuza RL, Rabkin SD, Johnson PA. 2001. Oncolytic herpes simplex virus vector with enhanced MHC class I presentation and tumor cell killing. PNAS 98:6396–401 [Google Scholar]
  143. Todo T, Feigenbaum F, Rabkin SD, Lakeman F, Newsome JT. et al. 2000.a Viral shedding and biodistribution of G207, a multimutated, conditionally replicating herpes simplex virus type 1, after intracebral inoculation in Aotus. Mol. Ther. 2:588–95 [Google Scholar]
  144. Todo T, Rabkin SD, Martuza RL. 2000.b Evaluation of ganciclovir-mediated enhancement of the antitumoral effect in oncolytic, multimutated herpes simplex virus type 1 (G207) therapy of brain tumors. Cancer Gene. Ther. 7:939–46 [Google Scholar]
  145. Tomazin R, Van Schoot NE Goldsmith K, Jugovic P, Sempe P. et al. 1998. Herpes simplex virus type 2 ICP47 inhibits human TAP but not mouse TAP. J. Virol. 72:2560–63 [Google Scholar]
  146. Trgovcich J, Johnson D, Roizman B. 2002. Cell surface major histocompatibility complex class II proteins are regulated by the products of the γ134.5 and UL41 genes of herpes simplex virus 1. J. Virol. 76:6974–86 [Google Scholar]
  147. van Lint AL, Murawski MR, Goodbody RE, Severa M, Fitzgerald KA. et al. 2010. Herpes simplex virus immediate-early ICP0 protein inhibits Toll-like receptor 2-dependent inflammatory responses and NF-κB signaling. J. Virol. 84:10802–11 [Google Scholar]
  148. Vere Hodge RA, Field HJ. 2013. Antiviral agents for herpes simplex virus. Adv. Pharmacol. 67:1–38 [Google Scholar]
  149. Verpooten D, Ma Y, Hou S, Yan Z, He B. 2009. Control of TANK-binding kinase 1-mediated signaling by the γ134.5 protein of herpes simplex virus 1. J. Biol. Chem. 284:1097–105 [Google Scholar]
  150. Viejo-Borbolla A, Martinez-Martin N, Nel HJ, Rueda P, Martin R. et al. 2012. Enhancement of chemokine function as an immunomodulatory strategy employed by human herpesviruses. PLOS Pathog 8:e1002497 [Google Scholar]
  151. Vogel K, Thomann S, Vogel B, Schuster P, Schmidt B. 2014. Both plasmacytoid dendritic cells and monocytes stimulate natural killer cells early during human herpes simplex virus type 1 infections. Immunology 143:588–600 [Google Scholar]
  152. Wakimoto H, Fulci G, Tyminski E, Chiocca EA. 2004. Altered expression of antiviral cytokine mRNAs associated with cyclophosphamide's enhancement of viral oncolysis. Gene. Ther. 11:214–23 [Google Scholar]
  153. Wakimoto H, Ikeda K, Abe T, Ichikawa T, Hochberg FH. et al. 2002. The complement response against an oncolytic virus is species-specific in its activation pathways. Mol. Ther. 5:275–82 [Google Scholar]
  154. Wakimoto H, Johnson PR, Knipe DM, Chiocca EA. 2003. Effects of innate immunity on herpes simplex virus and its ability to kill tumor cells. Gene. Ther. 10:983–90 [Google Scholar]
  155. Wakimoto H, Kesari S, Farrell CJ, Curry WT Jr., Zaupa C. et al. 2009. Human glioblastoma-derived cancer stem cells: establishment of invasive glioma models and treatment with oncolytic herpes simplex virus vectors. Cancer Res 69:3472–81 [Google Scholar]
  156. Walsh D, Mohr I. 2006. Assembly of an active translation initiation factor complex by a viral protein. Genes Dev 20:461–72 [Google Scholar]
  157. Wang K, Ni L, Wang S, Zheng C. 2014. Herpes simplex virus 1 protein kinase US3 hyperphosphorylates p65/RelA and dampens NF-κB activation. J. Virol. 88:7941–51 [Google Scholar]
  158. Wang S, Wang K, Li J, Zheng C. 2013.a Herpes simplex virus 1 ubiquitin-specific protease UL36 inhibits beta interferon production by deubiquitinating TRAF3. J. Virol. 87:11851–60 [Google Scholar]
  159. Wang S, Wang K, Lin R, Zheng C. 2013.b Herpes simplex virus 1 serine/threonine kinase US3 hyperphosphorylates IRF3 and inhibits beta interferon production. J. Virol. 87:12814–27 [Google Scholar]
  160. Wang Z, Choi MK, Ban T, Yanai H, Negishi H. et al. 2008. Regulation of innate immune responses by DAI (DLM-1/ZBP1) and other DNA-sensing molecules. PNAS 105:5477–82 [Google Scholar]
  161. Wilcox DR, Longnecker R. 2016. The herpes simplex virus neurovirulence factor γ34.5: revealing virus–host interactions. PLOS Pathog 12:e1005449 [Google Scholar]
  162. Wuest TR, Carr DJ. 2008. The role of chemokines during herpes simplex virus-1 infection. Front. Biosci. 13:4862–72 [Google Scholar]
  163. Xing J, Ni L, Wang S, Wang K, Lin R, Zheng C. 2013. Herpes simplex virus 1-encoded tegument protein VP16 abrogates the production of beta interferon (IFN) by inhibiting NF-κB activation and blocking IFN regulatory factor 3 to recruit its coactivator CBP. J. Virol. 87:9788–801 [Google Scholar]
  164. Xing J, Wang S, Lin R, Mossman KL, Zheng C. 2012. Herpes simplex virus 1 tegument protein US11 downmodulates the RLR signaling pathway via direct interaction with RIG-I and MDA-5. J. Virol. 86:3528–40 [Google Scholar]
  165. Xiong R, Rao P, Kim S, Li M, Wen X, Yuan W. 2015. Herpes simplex virus 1 US3 phosphorylates cellular KIF3A to downregulate CD1d expression. J. Virol. 89:6646–55 [Google Scholar]
  166. Yamada Y, Kimura H, Morishima T, Daikoku T, Maeno K, Nishiyama Y. 1991. The pathogenicity of ribonucleotide reductase-null mutants of herpes simplex virus type 1 in mice. J. Infect. Dis. 164:1091–97 [Google Scholar]
  167. Yang Y, Wu S, Wang Y, Pan S, Lan B. et al. 2015. The Us3 protein of herpes simplex virus 1 inhibits T cell signaling by confining linker for activation of t cells (LAT) activation via TRAF6 protein. J. Biol. Chem. 290:15670–78 [Google Scholar]
  168. Yokota S, Yokosawa N, Kubota T, Suzutani T, Yoshida I. et al. 2001. Herpes simplex virus type 1 suppresses the interferon signaling pathway by inhibiting phosphorylation of STATs and janus kinases during an early infection stage. Virology 286:119–24 [Google Scholar]
  169. Yokota S, Yokosawa N, Okabayashi T, Suzutani T, Miura S. et al. 2004. Induction of suppressor of cytokine signaling-3 by herpes simplex virus type 1 contributes to inhibition of the interferon signaling pathway. J. Virol. 78:6282–86 [Google Scholar]
  170. Yu X, He S. 2016. The interplay between human herpes simplex virus infection and the apoptosis and necroptosis cell death pathways. Virol. J. 13:77 [Google Scholar]
  171. Yuan M, Webb E, Lemoine NR, Wang Y. 2016. CRISPR-Cas9 as a powerful tool for efficient creation of oncolytic viruses. Viruses 8:72 [Google Scholar]
  172. Zenner HL, Mauricio R, Banting G, Crump CM. 2013. Herpes simplex virus 1 counteracts tetherin restriction via its virion host shutoff activity. J. Virol. 87:13115–23 [Google Scholar]
  173. Zevini A, Olagnier D, Hiscott J. 2017. Crosstalk between cytoplasmic RIG-I and STING sensing pathways. Trends Immunol 38:194–205 [Google Scholar]
  174. Zhang J, Wang K, Wang S, Zheng C. 2013.a Herpes simplex virus 1 E3 ubiquitin ligase ICP0 protein inhibits tumor necrosis factor alpha-induced NF-κB activation by interacting with p65/RelA and p50/NF-κB1. J. Virol. 87:12935–48 [Google Scholar]
  175. Zhang J, Wang S, Wang K, Zheng C. 2013.b Herpes simplex virus 1 DNA polymerase processivity factor UL42 inhibits TNF-α-induced NF-κB activation by interacting with p65/RelA and p50/NF-κB1. Med. Microbiol. Immunol. 202:313–25 [Google Scholar]
  176. Zhang SX. 2015. Turning killer into cure—the story of oncolytic herpes simplex viruses. Discov. Med. 20:303–9 [Google Scholar]
  177. Zhang W, Fulci G, Buhrman JS, Stemmer-Rachamimov AO, Chen JW. et al. 2012. Bevacizumab with angiostatin-armed oHSV increases antiangiogenesis and decreases bevacizumab-induced invasion in U87 glioma. Mol. Ther. 20:37–45 [Google Scholar]
  178. Zhang W, Fulci G, Wakimoto H, Cheema TA, Buhrman JS. et al. 2013. Combination of oncolytic herpes simplex viruses armed with angiostatin and IL-12 enhances antitumor efficacy in human glioblastoma models. Neoplasia 15:591–99 [Google Scholar]
  179. Zhou G, Roizman B. 2006. Construction and properties of a herpes simplex virus 1 designed to enter cells solely via the IL-13α2 receptor. PNAS 103:5508–13 [Google Scholar]
/content/journals/10.1146/annurev-cancerbio-030617-050254
Loading
Oncolytic Herpes Simplex Viruses as a Paradigm for the Treatment of Cancer
Annual Review of Cancer Biology 2, 155 (2018); https://doi.org/10.1146/annurev-cancerbio-030617-050254
/content/journals/10.1146/annurev-cancerbio-030617-050254
/content/journals/10.1146/annurev-cancerbio-030617-050254
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error