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Recombinant viruses with other anti-cancer therapeutics: a step towards advancement of oncolytic virotherapy

Cancer Gene Therapy volume 25, pages 216–226 (2018)Cite this article

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Abstract

Cancer as a disease is a multifaceted foe which sometimes succumbs to the prescribed treatment and sometimes develops resistance against various therapies. Conventional cancer therapies suffer from many limitations, the least of which is their specificity and systemic side effects. In a majority of cases, acquired mutations render the cancer cells resistant to therapy and lower the prognostic outcome. In the constant effort to devise a therapeutic moiety which can comprehensively eliminate cancer cells, oncolytic viruses provide an attractive avenue as they selectively infect and lyse cancer cells sparing normal cells from their effects. Viruses can be engineered for their host specificity and toxicity as a promising anti-cancer tool. As it is essential to devise a strategy to address all targets involved in cancer development and progression, the idea of using oncolytic viruses with enhanced anti-cancer activity through arming with foreign genes gained merit and is showing promising advent in clinical studies. The use of oncolytic viruses as an agent of combination therapy for cancer treatment also gained much attention in the recent past. This review focuses on the emerging role of oncolytic viruses as vital components of anti-cancer regimen presenting a new dimension in an ever-changing cancer therapy scenario.

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References

  1. Housman G, Byler S, Heerboth S, Longacre M, Snyder N, Sarkar S. Drug resistance in cancer: an overview. Cancers (Basel). 2014;6:1769–92.

    Article  CAS  Google Scholar 

  2. Das SK, Menezes ME, Bhatia S, Wang X-Y, Emdad L, Sarkar D, et al. Gene therapies for cancer: strategies, challenges and successes. J Cell Physiol. 2015;230:259–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Bluming A, Ziegler J. Regression of Burkitt’s lymphoma in association with Measles infection. Lancet. 1971;298:105–6.

    Article  Google Scholar 

  4. Hansen RM, Libnoch JA. Remission of chronic lymphocytic leukemia after smallpox vaccination. Arch Intern Med. 1978;138:1137–8.

    Article  CAS  PubMed  Google Scholar 

  5. Russell SJ, Peng KW. Viruses as anticancer drugs. Trends Pharmacol Sci. 2007;28:326–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Russell SJ, Peng K-W, Bell JC. Oncolytic virotherapy. Nat Biotechnol. 2012;30:658–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Toro Bejarano M, Merchan JR. Targeting tumor vasculature through oncolytic virotherapy: recent advances. Oncolytic Virother. 2015;4:169–81.

    PubMed  PubMed Central  Google Scholar 

  8. Loskog A. Immunostimulatory gene therapy using oncolytic viruses as vehicles. Viruses. 2015;7:5780–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Grote D, Russell SJ, Cornu TI, Cattaneo R, Vile R, Poland GA, et al. Live attenuated measles virus induces regression of human lymphoma xenografts in immunodeficient mice. Blood. 2001;97:3746–54.

    Article  CAS  PubMed  Google Scholar 

  10. Russell SJ, Peng KW. Measles virus for cancer therapy. Curr Top Microbiol Immunol. 2009;330:213–41.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Antonio Chiocca E. Oncolytic viruses. Nat Rev Cancer. 2002;2:938–50.

    Article  CAS  PubMed  Google Scholar 

  12. Peng Z. Current status of gendicine in China: recombinant human Ad-p53 agent for treatment of cancers. Hum Gene Ther. 2005;16:1016–27.

    Article  CAS  PubMed  Google Scholar 

  13. Wong HH, Lemoine NR, Wang Y. Oncolytic viruses for cancer therapy: overcoming the obstacles. Viruses. 2010;2:78–106.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Yang L, Pang Y, Moses HL. TGF-β and immune cells: an important regulatory axis in the tumor microenvironment and progression. Trends Immunol. 2010;31:220–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Naik S, Nace R, Federspiel MJ, Barber GN, Peng K-W, Russell SJ. Curative one-shot systemic virotherapy in murine myeloma. Leukemia. 2012;26:1870–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Hu JCC, Coffin RS, Davis CJ, Graham NJ, Groves N, Guest PJ, 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 LP–6747.

    Article  Google Scholar 

  17. Seubert CM, Stritzker J, Hess M, Donat U, Sturm JB, Chen N, et al. Enhanced tumor therapy using vaccinia virus strain GLV-1h68 in combination with a β-galactosidase-activatable prodrug seco-analog of duocarmycin SA. Cancer Gene Ther. 2011;18:42–52.

    Article  CAS  PubMed  Google Scholar 

  18. Wei D, Li Q, Wang X-L, Wang Y, Xu J, Feng F, et al. Oncolytic Newcastle disease virus expressing chimeric antibody enhanced anti-tumor efficacy in orthotopic hepatoma-bearing mice. J Exp Clin Cancer Res. 2015;34:153.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Nistal-Villan E, Bunuales M, Poutou J, Gonzalez-Aparicio M, Bravo-Perez C, Quetglas JI, et al. Enhanced therapeutic effect using sequential administration of antigenically distinct oncolytic viruses expressing oncostatin M in a Syrian hamster orthotopic pancreatic cancer model. Mol Cancer. 2015;14:210.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Mccart JA, Puhlmann M, Lee J, Hu Y, Libutti SK, Alexander HR, et al. Complex interactions between the replicating oncolytic effect and the enzyme / prodrug effect of vaccinia- mediated tumor regression. Cancer Gene Ther. 2000;7:1217–23.

    CAS  Google Scholar 

  21. Dingli D, Peng K-W, Harvey ME, Vongpunsawad S, Bergert ER, Kyle RA, et al. Interaction of measles virus vectors with Auger electron emitting radioisotopes. Biochem Biophys Res Commun. 2005;337:22–29.

    Article  CAS  PubMed  Google Scholar 

  22. Advani SJ, Sibley GS, Song PY, Hallahan DE, Kataoka Y, Roizman B, 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;5:160–5.

    Article  CAS  PubMed  Google Scholar 

  23. Blank SV, Rubin SC, Coukos G, Amin KM, Albelda SM, Molnar-Kimber KL. Replication-selective herpes simplex virus type 1 mutant therapy of cervical cancer is enhanced by low-dose radiation. Hum Gene Ther. 2002;13:627–39.

    Article  CAS  PubMed  Google Scholar 

  24. Stanziale SF, Petrowsky H, Joe JK, Roberts GD, Zager JS, Gusani NJ, et al. Ionizing radiation potentiates the antitumor efficacy of oncolytic herpes simplex virus G207 by upregulating ribonucleotide reductase. Surgery. 2002;132:353–9.

    Article  PubMed  Google Scholar 

  25. Adusumilli PS, Stiles BM, Chan MK, Chou TC, Wong RJ, Rusch VW, et al. Radiation therapy potentiates effective oncolytic viral therapy in the treatment of lung cancer. Ann Thorac Surg. 2005;80:409–16..

    Article  PubMed  PubMed Central  Google Scholar 

  26. Adusumilli PS, Chan MK, Hezel M, Yu Z, Stiles BM, Chou TC, et al. Radiation-induced cellular DNA damage repair response enhances viral gene therapy efficacy in the treatment of malignant pleural mesothelioma. Ann Surg Oncol. 2007;14:258–69..

    Article  PubMed  Google Scholar 

  27. Advani SJ, Markert JM, Sood RF, Samuel S, Gillespie GY, Shao MY, et al. Increased oncolytic efficacy for high-grade gliomas by optimal integration of ionizing radiation into the replicative cycle of HSV-1. Gene Ther. 2011;18:1098–102.

    Article  CAS  PubMed  Google Scholar 

  28. Liu C, JN S, CA P, Paraskevakou G, PJ Z, Schroeder M. Combination of measles virus virotherapy and radiation therapy has synergistic activity in the treatment of glioblastoma multiforme. Clin Cancer Res. 2007;12:7155–65.

    Article  Google Scholar 

  29. Idema S, Lamfers MLM, van Beusechem VW, Noske DP, Heukelom S, Moeniralm S, et al. AdΔ24 and the p53-expressing variant AdΔ24-p53 achieve potent anti-tumor activity in glioma when combined with radiotherapy. J Gene Med. 2007;9:1046–56.

    Article  CAS  PubMed  Google Scholar 

  30. Rogulski KR, Wing MS, Paielli DL, Gilbert JD, Kim JH, Freytag SO. 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.

    Article  CAS  PubMed  Google Scholar 

  31. Portella G, Pacelli R, Libertini S, Cella L, Vecchio G, Salvatore M, et al. ONYX-015 enhances radiation-induced death of human anaplastic thyroid carcinoma cells. J Clin Endocrinol Metab. 2003;88:5027–32.

    Article  CAS  PubMed  Google Scholar 

  32. Geoerger B, Grill J, Opolon P, Morizet J, Aubert G, Lecluse Y, et al. Potentiation of radiation therapy by the oncolytic adenovirusdl1520 (ONYX-015) in human malignant glioma xenografts. Br J Cancer. 2003;89:577–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Chen Y, DeWeese T, Dilley J, Zhang Y, Li Y, Ramesh N, 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 LP–5460.

    Google Scholar 

  34. Dilley J, Reddy S, Ko D, Nguyen N, Rojas G, Working P. Oncolytic adenovirus CG7870 in combination with radiation demonstrates synergistic enhancements of antitumor efficacy without loss of specificity. Cancer Gene Ther. 2005;12:715–22.

    Article  CAS  PubMed  Google Scholar 

  35. Ma G, Shimada H, Hiroshima K, Tada Y, Suzuki N, Tagawa M. Gene medicine for cancer treatment: commercially available medicine and accumulated clinical data in China. Drug Des Devel Ther. 2008;2:115–22.

    CAS  Google Scholar 

  36. Blanchard M, Shim KG, Grams MP, Rajani K, Diaz RM, Furutani KM, et al. Definitive management of oligometastatic melanoma in a murine model using combined ablative radiation therapy and viral immunotherapy. Int J Radiat Oncol Biol Phys. 2015;93:577–87.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Twigger K, Vidal L, White CL, De Bono JS, Bhide S, Coffey M. et al. Enhanced in vitro and in vivo cytotoxicity of combined reovirus and radiotherapy. Clin Cancer Res. 2008;14:912–23.

    Article  CAS  PubMed  Google Scholar 

  38. McEntee G, Kyula JN, Mansfield D, Smith H, Wilkinson M, Gregory C, et al. Enhanced cytotoxicity of reovirus and radiotherapy in melanoma cells is mediated through increased viral replication and mitochondrial apoptotic signalling. Oncotarget. 2016;7:48517–32.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Wilkinson MJ, Smith HG, McEntee G, Kyula-Currie J, Pencavel TD, Mansfield DC, et al. Oncolytic vaccinia virus combined with radiotherapy induces apoptotic cell death in sarcoma cells by down-regulating the inhibitors of apoptosis. Oncotarget. 2016;7:81208–22.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Lee W-P, Tai D-I, Tsai S-L, Yeh C-T, Chao Y, Lee S-D, et al. Adenovirus type 5 E1A sensitizes hepatocellular carcinoma cells to gemcitabine. Cancer Res. 2003;63:6229 LP–6236.

    Google Scholar 

  41. Guan YS, Sun L, Zhou XP, et al. Combination therapy with recombinant adenovirus-p53 injection (rAd-p53) via transcatheter hepatic arterial chemoembolization for advanced hepatic carcinoma. Shijie Huaren Xiaohua Zazhi. 2005;13:125–7.

    Google Scholar 

  42. Xia Z-J, Chang J-H, Zhang L, Jiang W-Q, Guan Z-Z, Liu J-W, et al. [Phase III randomized clinical trial of intratumoral injection of E1B gene-deleted adenovirus (H101) combined with cisplatin-based chemotherapy in treating squamous cell cancer of head and neck or esophagus]. Ai Zheng. 2004;23:1666–70.

    PubMed  Google Scholar 

  43. Nemunaitis J, Clayman G, Agarwala SS, Hrushesky W, Wells JR, Moore C, et al. Biomarkers predict p53 gene therapy efficacy in recurrent squamous cell carcinoma of the head and neck. Clin Cancer Res. 2009;; 15:7719 LP–7725.

    Article  Google Scholar 

  44. Kangasniemi L, Parviainen S, Pisto T, Koskinen M, Jokinen M, Kiviluoto T, et al. Effects of capsid-modified oncolytic adenoviruses and their combinations with gemcitabine or silica gel on pancreatic cancer. Int J Cancer. 2012;131:253–63.

    Article  CAS  PubMed  Google Scholar 

  45. Pesonen S, Diaconu I, Cerullo V, Escutenaire S, Raki M, Kangasniemi L, et al. Integrin targeted oncolytic adenoviruses Ad5-D24-RGD and Ad5-RGD-D24-GMCSF for treatment of patients with advanced chemotherapy refractory solid tumors. Int J Cancer. 2012;130:1937–47.

    Article  CAS  PubMed  Google Scholar 

  46. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Roulstone V, Khan K, Pandha HS, Rudman S, Coffey M, Gill GM, et al. Phase I trial of cyclophosphamide as an immune modulator for optimizing oncolytic reovirus delivery to solid tumors. Clin Cancer Res. 2015;21:1305–12.

    Article  CAS  PubMed  Google Scholar 

  48. Lolkema MP, Arkenau H-T, Harrington K, Roxburgh P, Morrison R, Roulstone V, et al. 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 LP–588.

    Article  Google Scholar 

  49. Karapanagiotou EM, Roulstone V, Twigger K, Ball M, Tanay MA, Nutting C, 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;18:2080–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Adusumilli PS, Chan M-K, Chun YS, Hezel M, Chou T-C, Rusch VW, et al. Cisplatin-induced GADD34 upregulation potentiates oncolytic viral therapy in the treatment of malignant pleural mesothelioma. Cancer Biol Ther. 2006;5:48–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Bourgeois-Daigneault M-C, St-Germain LE, Roy DG, Pelin A, Aitken AS, Arulanandam R, et al. Combination of paclitaxel and MG1 oncolytic virus as a successful strategy for breast cancer treatment. Breast Cancer Res. 2016;18:83.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Al-Shammari AM, Rameez H, Al-Taee MF. Newcastle disease virus, rituximab, and doxorubicin combination as anti-hematological malignancy therapy. Oncolytic Virother. 2016;5:27–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Hofmann E, Weibel S, Szalay AA. Combination treatment with oncolytic Vaccinia virus and cyclophosphamide results in synergistic antitumor effects in human lung adenocarcinoma bearing mice. J Transl Med. 2014;12:197.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Wang H, Chen NG, Minev BR, Szalay AA. Oncolytic vaccinia virus GLV-1h68 strain shows enhanced replication in human breast cancer stem-like cells in comparison to breast cancer cells. J Transl Med. 2012;10:167.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Yu Z, Li S, Brader P, Chen N, Yu YA, Zhang Q, et al. Oncolytic vaccinia therapy of squamous cell carcinoma. Mol Cancer. 2009;8:45.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Chernichenko N, Linkov G, Li P, Bakst RL, Chen C-H, He S, et al. Oncolytic vaccinia virus therapy of salivary gland carcinoma. JAMA Otolaryngol Head Neck Surg. 2013;139:173–82.

    Article  PubMed  PubMed Central  Google Scholar 

  57. He S, Li P, Chen C-H, Bakst RL, Chernichenko N, Yu YA, et al. Effective oncolytic vaccinia therapy for human sarcomas. J Surg Res. 2012;175:e53–e60.

    Article  PubMed  Google Scholar 

  58. Garber K. HDAC inhibitors overcome first hurdle. Nat Biotech. 2007;25:17–19.

    Article  CAS  Google Scholar 

  59. Bressy C, Hastie E, Grdzelishvili VZ. Combining oncolytic virotherapy with p53 tumor suppressor gene therapy. Mol Ther Oncolytics. 2017;5:20–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Marchini A, Scott EM, Rommelaere J. Overcoming barriers in oncolytic virotherapy with HDAC inhibitors and immune checkpoint blockade. Viruses. 2016;8:pii: E9

    Article  Google Scholar 

  61. Nguyen TL-A, Abdelbary H, Arguello M, Breitbach C, Leveille S, Diallo J-S, et al. Chemical targeting of the innate antiviral response by histone deacetylase inhibitors renders refractory cancers sensitive to viral oncolysis. Proc Natl Acad Sci USA. 2008;105:14981–6.

    Article  CAS  PubMed  Google Scholar 

  62. Goldsmith ME, Aguila A, Steadman K, Martinez A, Steinberg SM, Alley MC, et al. The histone deacetylase inhibitor FK228 given prior to adenovirus infection can boost infection in melanoma xenograft model systems. Mol Cancer Ther. 2007;6:496 LP–505.

    Article  Google Scholar 

  63. Berghauser Pont LM, Kleijn A, Kloezeman JJ, van den Bossche W, Kaufmann JK, de Vrij J, et al. The HDAC inhibitors scriptaid and LBH589 combined with the oncolytic virus Delta24-RGD exert enhanced anti-tumor efficacy in patient-derived glioblastoma cells. PLoS ONE. 2015;10:1–20.

    Article  Google Scholar 

  64. Liu T-C, Castelo Branco P, Rabkin SD, Martuza RL. Trichostatin A and oncolytic HSV combination therapy shows enhanced antitumoral and antiangiogenic effects. Mol Ther. 2008;16:1041–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Schipper H, Alla V, Meier C, Nettelbeck DM, Herchenroder O, Putzer BM. Eradication of metastatic melanoma through cooperative expression of RNA-based HDAC1 inhibitor and p73 by oncolytic adenovirus. Oncotarget. 2014;5:5893–907.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Bartlett DL, Liu Z, Sathaiah M, Ravindranathan R, Guo Z, He Y, et al. Oncolytic viruses as therapeutic cancer vaccines. Mol Cancer. 2013;12:103.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Guo ZS, Liu Z, Bartlett DL. Oncolytic Immunotherapy: dying the right way is a key to eliciting potent antitumor immunity. Front Oncol. 2014;4:74.

    PubMed  PubMed Central  Google Scholar 

  68. Bauzon M, Hermiston T. Armed therapeutic viruses - a disruptive therapy on the horizon of cancer immunotherapy. Front Immunol. 2014;5:1–10.

    Article  CAS  Google Scholar 

  69. Gao Y, Whitaker-Dowling P, Griffin JA, Barmada MA, Bergman I. Recombinant vesicular stomatitis virus targeted to Her2/neu combined with anti-CTLA4 antibody eliminates implanted mammary tumors. Cancer Gene Ther. 2008;16:44–52.

    Article  PubMed  Google Scholar 

  70. Zamarin D, Holmgaard RB, Subudhi SK, Park JS, Mansour M, Palese P, et al. Localized oncolytic virotherapy overcomes systemic tumor resistance to immune checkpoint blockade immunotherapy. Sci Transl Med. 2014;6:226ra32

    Article  PubMed  PubMed Central  Google Scholar 

  71. Puzanov I, Milhem M, Andtbacka R, Minor D, Hamid O, Li A, et al. Phase 1 results of a phase 1b/2, multicenter, open-label trial to evaluate safety and efficacy of talimogene laherparepvec (T-VEC) and ipilimumab (ipi) vs ipi alone in previously untreated, unresected stage IIIB-IV melanoma. J Immunother Cancer. 2013;1:P84–P84.

    Article  PubMed Central  Google Scholar 

  72. Kleinpeter P, Fend L, Thioudellet C, Geist M, Sfrontato N, Koerper V, et al. Vectorization in an oncolytic vaccinia virus of an antibody, a Fab and a scFv against programmed cell death -1 (PD-1) allows their intratumoral delivery and an improved tumor-growth inhibition. Oncoimmunology. 2016;5:e1220467.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Dias JD, Hemminki O, Diaconu I, Hirvinen M, Bonetti A, Guse K, et al. Targeted cancer immunotherapy with oncolytic adenovirus coding for a fully human monoclonal antibody specific for CTLA-4. Gene Ther. 2012;19:988–98.

    Article  CAS  PubMed  Google Scholar 

  74. Engeland CE, Grossardt C, Veinalde R, Bossow S, Lutz D, Kaufmann JK, et al. CTLA-4 and PD-L1 checkpoint blockade enhances oncolytic measles virus therapy. Mol Ther. 2014;22:1949–59.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Jiang H, Rivera-Molina Y, Clise-Dwyer K, Bover L, Vence L, Yuan Y, et al. Oncolytic adenovirus and tumor-targeting immune modulatory therapy improve autologous cancer vaccination. Cancer Res. 2017;77:3894–3907.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Ottolino-Perry K, Diallo J-S, Lichty BD, Bell JC, McCart JA. Intelligent design: combination therapy with oncolytic viruses. Mol Ther. 2010;18:251–63.

    Article  CAS  PubMed  Google Scholar 

  77. Ilett E, Kottke T, Thompson J, Rajani K, Zaidi S, Evgin L, et al. Prime-boost using separate oncolytic viruses in combination with checkpoint blockade improves anti-tumor therapy. Gene Ther. 2017;24:21–30.

    Article  CAS  PubMed  Google Scholar 

  78. Suzuki K, Fueyo J, Krasnykh V, Reynolds PN, Curiel DT, Alemany R. A conditionally replicative adenovirus with enhanced infectivity shows improved oncolytic potency. Clin Cancer Res. 2001;7:120 LP–126.

    Google Scholar 

  79. Yang Y, Xu H, Shen J, Yang Y, Wu S, Xiao J, et al. RGD-modifided oncolytic adenovirus exhibited potent cytotoxic effect on CAR-negative bladder cancer-initiating cells. Cell Death Dis. 2015;6:e1760.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Yamamoto Y, Hiraoka N, Goto N, Rin Y, Miura K, Narumi K, et al. A targeting ligand enhances infectivity and cytotoxicity of an oncolytic adenovirus in human pancreatic cancer tissues. J Control Release. 2014;192:284–93.

    Article  CAS  PubMed  Google Scholar 

  81. Yamamoto Y, Nagasato M, Rin Y, Henmi M, Ino Y, Yachida S, et al. Strong antitumor efficacy of a pancreatic tumor-targeting oncolytic adenovirus for neuroendocrine tumors. Cancer Med. 2017;6:2385–97.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Nokisalmi P, Pesonen S, Escutenaire S, Ristimki A, Joensuu T, Guse K, et al. Clinical data from cancer patients treated with triple modified oncolytic adenovirus Ad5/3-Cox2L-D24. Hum Gene Ther. 2008;19:1076.

    Article  Google Scholar 

  83. Pesonen S, Nokisalmi P, Escutenaire S, Sarkioja M, Raki M, Cerullo V, et al. Prolonged systemic circulation of chimeric oncolytic adenovirus Ad5/3-Cox2L-D24 in patients with metastatic and refractory solid tumors. Gene Ther. 2010;17:892–904.

    Article  CAS  PubMed  Google Scholar 

  84. Yu D, Jin C, Leja J, Majdalani N, Nilsson B, Eriksson F, et al. Adenovirus with hexon Tat-protein transduction domain modification exhibits increased therapeutic effect in experimental neuroblastoma and neuroendocrine tumors. J Virol. 2011;85:13114–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Hsiao W-C, Sung S-Y, Liao C-H, Wu H-C, Hsieh C-L. Vitamin D3-inducible mesenchymal stem cell-based delivery of conditionally replicating adenoviruses effectively targets renal cell carcinoma and inhibits tumor growth. Mol Pharm. 2012;9:1396–408.

    Article  CAS  PubMed  Google Scholar 

  86. Lu C-S, Hsieh J-L, Lin C-Y, Tsai H-W, Su B-H, Shieh G-S, et al. Potent antitumor activity of Oct4 and hypoxia dual-regulated oncolytic adenovirus against bladder cancer. Gene Ther. 2015;22:305–15.

    Article  CAS  PubMed  Google Scholar 

  87. Fajardo CA, Guedan S, Rojas LA, Moreno R, Arias-Badia M, de Sostoa J, et al. Oncolytic adenoviral delivery of an EGFR-targeting T-cell engager improves antitumor efficacy. Cancer Res. 2017;77:2052 LP–2063.

    Article  Google Scholar 

  88. Friedrich K, Hanauer JR, Prüfer S, Münch RC, Völker I, Filippis C, et al. DARPin-targeting of measles virus: unique bispecificity, effective oncolysis, and enhanced safety. Mol Ther. 2013;21:849–59.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Paraskevakou G, Allen C, Nakamura T, Zollman P, James CD, Peng KW, et al. Epidermal growth factor receptor (EGFR)– retargeted measles virus strains effectively target EGFR- or EGFRvIII expressing gliomas. Mol Ther J Am Soc Gene Ther. 2007;15:677–86.

    Article  CAS  Google Scholar 

  90. Hanauer JR, Gottschlich L, Riehl D, Rusch T, Koch V, Friedrich K, et al. Enhanced lysis by bispecific oncolytic measles viruses simultaneously using HER2/neu or EpCAM as target receptors. Mol Ther Oncolytics. 2016;3:16003.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Guillerme JB, Gregoire M, Tangy F, Fonteneau JF. Antitumor virotherapy by attenuated measles virus (MV). Biology (Basel). 2013;2:587–602.

    CAS  Google Scholar 

  92. Amagai Y, Fujiyuki T, Yoneda M, Shoji K, Furukawa Y, Sato H, et al. Oncolytic activity of a recombinant measles virus, blind to signaling lymphocyte activation molecule, against colorectal cancer cells. Sci Rep. 2016;6:24572.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Fujiyuki T, Yoneda M, Amagai Y, Obayashi K, Ikeda F, Shoji K, et al. A measles virus selectively blind to signaling lymphocytic activation molecule shows anti-tumor activity against lung cancer cells. Oncotarget. 2015;6:24895–903.

    Article  PubMed  PubMed Central  Google Scholar 

  94. Jing Y, Bejarano MT, Zaias J, Merchan JR. In vivo anti-metastatic effects of uPAR retargeted measles virus in syngeneic and xenograft models of mammary cancer. Breast Cancer Res Treat. 2015;149:99–108.

    Article  PubMed  Google Scholar 

  95. Miest TS, Yaiw K-C, Frenzke M, Lampe J, Hudacek AW, Springfeld C, et al. Envelope-chimeric entry-targeted measles virus escapes neutralization and achieves oncolysis. Mol Ther. 2011;19:1813–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Leoni V, Gatta V, Palladini A, Nicoletti G, Ranieri D, Dall’Ora M, et al. Systemic delivery of HER2-retargeted oncolytic-HSV by mesenchymal stromal cells protects from lung and brain metastases. Oncotarget. 2015;6:34774–87.

    Article  PubMed  PubMed Central  Google Scholar 

  97. Gatta V, Petrovic B, Campadelli-Fiume G. The engineering of a novel ligand in gH confers to HSV an expanded tropism independent of gD activation by its receptors. PLoS Pathog. 2015;11:e1004907.

    Article  PubMed  PubMed Central  Google Scholar 

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    Geetanjali Lal & Maitreyi S. Rajala

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Lal, G., Rajala, M.S. Recombinant viruses with other anti-cancer therapeutics: a step towards advancement of oncolytic virotherapy. Cancer Gene Ther 25, 216–226 (2018). https://doi.org/10.1038/s41417-018-0018-1

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  • DOI: https://doi.org/10.1038/s41417-018-0018-1

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