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Current Pharmaceutical Design

Author(s): Yuhui Zhang* and Zhuoming Liu*

DOI: 10.2174/1381612825666191104090544

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Oncolytic Virotherapy for Malignant Tumor: Current Clinical Status

Page: [4251 - 4263] Pages: 13

  • * (Excluding Mailing and Handling)

Abstract

Oncolytic viruses, as novel biological anti-tumor agents, provide anti-tumor therapeutic effects by different mechanisms including directly selective tumor cell lysis and secondary systemic anti-tumor immune responses. Some wide-type and genetically engineered oncolytic viruses have been applied in clinical trials. Among them, T-Vec has a significant therapeutic effect on melanoma patients and received the approval of the US Food and Drug Administration (FDA) as the first oncolytic virus to treat cancer in the US. However, the mechanisms of virus interaction with tumor and immune systems have not been clearly elucidated and there are still no “gold standards” for instructions of virotherapy in clinical trials. This Review collected the recent clinical trials data from 2005 to summarize the basic oncolytic viruses biology, describe the application in recent clinical trials, and discuss the challenges in the application of oncolytic viruses in clinical trials.

Keywords: Virotherapy, cancer, malignant tumor, clinical trial, genetically engineered, oncolytic viruses.

[1]
Russell SJ, Peng KW. Viruses as anticancer drugs. Trends Pharmacol Sci 2007; 28(7): 326-33.
[http://dx.doi.org/10.1016/j.tips.2007.05.005] [PMID: 17573126]
[2]
Kelly E, Russell SJ. History of oncolytic viruses: genesis to genetic engineering. Mol Ther 2007; 15(4): 651-9.
[http://dx.doi.org/10.1038/sj.mt.6300108] [PMID: 17299401]
[3]
Roberts MS, Lorence RM, Groene WS, Bamat MK. Naturally oncolytic viruses. Curr Opin Mol Ther 2006; 8(4): 314-21.
[PMID: 16955694]
[4]
Bourhill T, Mori Y, Rancourt DE, Shmulevitz M, Johnston RN. Going (Reo)viral: factors promoting successful reoviral oncolytic infection. Viruses 2018; 10(8): 10.
[http://dx.doi.org/10.3390/v10080421] [PMID: 30103501]
[5]
Dorer DE, Nettelbeck DM. Targeting cancer by transcriptional control in cancer gene therapy and viral oncolysis. Adv Drug Deliv Rev 2009; 61(7-8): 554-71.
[http://dx.doi.org/10.1016/j.addr.2009.03.013] [PMID: 19394376]
[6]
Russell SJ, Peng KW. Oncolytic virotherapy: a contest between apples and oranges. Mol Ther 2017; 25(5): 1107-16.
[http://dx.doi.org/10.1016/j.ymthe.2017.03.026] [PMID: 28392162]
[7]
Fukazawa T, Matsuoka J, Yamatsuji T, Maeda Y, Durbin ML, Naomoto Y. Adenovirus-mediated cancer gene therapy and virotherapy. (Review) Int J Mol Med 2010; 25(1): 3-10.
[PMID: 19956895]
[8]
Zeyaullah M, Patro M, Ahmad I, et al. Oncolytic viruses in the treatment of cancer: a review of current strategies. Pathol Oncol Res 2012; 18(4): 771-81.
[http://dx.doi.org/10.1007/s12253-012-9548-2] [PMID: 22714538]
[9]
Vähä-Koskela MJ, Heikkilä JE, Hinkkanen AE. Oncolytic viruses in cancer therapy. Cancer Lett 2007; 254(2): 178-216.
[http://dx.doi.org/10.1016/j.canlet.2007.02.002] [PMID: 17383089]
[10]
Kelly EJ, Russell SJ. MicroRNAs and the regulation of vector tropism. Mol Ther 2009; 17(3): 409-16.
[http://dx.doi.org/10.1038/mt.2008.288] [PMID: 19107117]
[11]
Waehler R, Russell SJ, Curiel DT. Engineering targeted viral vectors for gene therapy. Nat Rev Genet 2007; 8(8): 573-87.
[http://dx.doi.org/10.1038/nrg2141] [PMID: 17607305]
[12]
Pelner L, Fowler GA, Nauts HC. Effects of concurrent infections and their toxins on the course of leukemia. Acta Med Scand Suppl 1958; 338: 1-47.
[http://dx.doi.org/10.1111/j.0954-6820.1958.tb17327.x] [PMID: 13605619]
[13]
Murphy AM, Rabkin SD. Current status of gene therapy for brain tumors. Transl Res 2013; 161(4): 339-54.
[http://dx.doi.org/10.1016/j.trsl.2012.11.003] [PMID: 23246627]
[14]
Jiang H, Gomez-Manzano C, Rivera-Molina Y, Lang FF, Conrad CA, Fueyo J. Oncolytic adenovirus research evolution: from cell-cycle checkpoints to immune checkpoints. Curr Opin Virol 2015; 13: 33-9.
[http://dx.doi.org/10.1016/j.coviro.2015.03.009] [PMID: 25863716]
[15]
Bischoff JR, Kirn DH, Williams A, et al. An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science 1996; 274(5286): 373-6.
[http://dx.doi.org/10.1126/science.274.5286.373] [PMID: 8832876]
[16]
Rao L, Debbas M, Sabbatini P, Hockenbery D, Korsmeyer S, White E. The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kDa and Bcl-2 proteins. Proc Natl Acad Sci USA 1992; 89(16): 7742-6.
[http://dx.doi.org/10.1073/pnas.89.16.7742] [PMID: 1457005]
[17]
Fueyo J, Gomez-Manzano C, Alemany R, et al. A mutant oncolytic adenovirus targeting the Rb pathway produces anti-glioma effect in vivo. Oncogene 2000; 19(1): 2-12.
[http://dx.doi.org/10.1038/sj.onc.1203251] [PMID: 10644974]
[18]
Chiocca EA, Rabkin SD. Oncolytic viruses and their application to cancer immunotherapy. Cancer Immunol Res 2014; 2(4): 295-300.
[http://dx.doi.org/10.1158/2326-6066.CIR-14-0015] [PMID: 24764576]
[19]
Kaur B, Chiocca EA, Cripe TP. Oncolytic HSV-1 virotherapy: clinical experience and opportunities for progress. Curr Pharm Biotechnol 2012; 13(9): 1842-51.
[http://dx.doi.org/10.2174/138920112800958814] [PMID: 21740359]
[20]
Nakashima H, Kaufmann JK, Wang PY, et al. Histone deacetylase 6 inhibition enhances oncolytic viral replication in glioma. J Clin Invest 2015; 125(11): 4269-80.
[http://dx.doi.org/10.1172/JCI80713] [PMID: 26524593]
[21]
Alcantara Llaguno S, Chen J, Kwon CH, et al. Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell 2009; 15(1): 45-56.
[http://dx.doi.org/10.1016/j.ccr.2008.12.006] [PMID: 19111880]
[22]
Stepanenko AA, Chekhonin VP. Recent advances in oncolytic virotherapy and immunotherapy for glioblastoma: a glimmer of hope in the search for an effective therapy? Cancers (Basel) 2018; 10(12): 10.
[http://dx.doi.org/10.3390/cancers10120492] [PMID: 30563098]
[23]
Conrad C, Miller CR, Ji Y, et al. Delta24-hyCD adenovirus suppresses glioma growth in vivo by combining oncolysis and chemosensitization. Cancer Gene Ther 2005; 12(3): 284-94.
[http://dx.doi.org/10.1038/sj.cgt.7700750] [PMID: 15650766]
[24]
Gomez-Manzano C, Balague C, Alemany R, et al. A novel E1A-E1B mutant adenovirus induces glioma regression in vivo. Oncogene 2004; 23(10): 1821-8.
[http://dx.doi.org/10.1038/sj.onc.1207321] [PMID: 15014451]
[25]
Cancer Genome Atlas Research Network. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008; 455(7216): 1061-8.
[http://dx.doi.org/10.1038/nature07385] [PMID: 18772890]
[26]
Bergelson JM, Cunningham JA, Droguett G, et al. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 1997; 275(5304): 1320-3.
[http://dx.doi.org/10.1126/science.275.5304.1320] [PMID: 9036860]
[27]
Martino TA, Petric M, Weingartl H, et al. The coxsackie-adenovirus receptor (CAR) is used by reference strains and clinical isolates representing all six serotypes of coxsackievirus group B and by swine vesicular disease virus. Virology 2000; 271(1): 99-108.
[http://dx.doi.org/10.1006/viro.2000.0324] [PMID: 10814575]
[28]
Coyne CB, Bergelson JM. CAR: a virus receptor within the tight junction. Adv Drug Deliv Rev 2005; 57(6): 869-82.
[http://dx.doi.org/10.1016/j.addr.2005.01.007] [PMID: 15820557]
[29]
Fueyo J, Alemany R, Gomez-Manzano C, et al. Preclinical characterization of the antiglioma activity of a tropism-enhanced adenovirus targeted to the retinoblastoma pathway. J Natl Cancer Inst 2003; 95(9): 652-60.
[http://dx.doi.org/10.1093/jnci/95.9.652] [PMID: 12734316]
[30]
Jiang H, Clise-Dwyer K, Ruisaard KE, et al. Delta-24-RGD oncolytic adenovirus elicits anti-glioma immunity in an immunocompetent mouse model. PLoS One 2014; 9(5) e97407
[http://dx.doi.org/10.1371/journal.pone.0097407] [PMID: 24827739]
[31]
Barnett BG, Crews CJ, Douglas JT. Targeted adenoviral vectors. Biochim Biophys Acta 2002; 1575(1-3): 1-14.
[http://dx.doi.org/10.1016/S0167-4781(02)00249-X] [PMID: 12020813]
[32]
Kaur S, Kenny HA, Jagadeeswaran S, et al. beta3-integrin expression on tumor cells inhibits tumor progression, reduces metastasis, and is associated with a favorable prognosis in patients with ovarian cancer. Am J Pathol 2009; 175(5): 2184-96.
[http://dx.doi.org/10.2353/ajpath.2009.090028] [PMID: 19808644]
[33]
Wickham TJ, Mathias P, Cheresh DA, Nemerow GR. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 1993; 73(2): 309-19.
[http://dx.doi.org/10.1016/0092-8674(93)90231-E] [PMID: 8477447]
[34]
Shayakhmetov DM, Lieber A. Dependence of adenovirus infectivity on length of the fiber shaft domain. J Virol 2000; 74(22): 10274-86.
[http://dx.doi.org/10.1128/JVI.74.22.10274-10286.2000] [PMID: 11044071]
[35]
Takagi-Kimura M, Yamano T, Tamamoto A, et al. Enhanced antitumor efficacy of fiber-modified, midkine promoter-regulated oncolytic adenovirus in human malignant mesothelioma. Cancer Sci 2013; 104(11): 1433-9.
[http://dx.doi.org/10.1111/cas.12267] [PMID: 23962292]
[36]
Uusi-Kerttula H, Hulin-Curtis S, Davies J, Parker AL. Oncolytic Adenovirus: strategies and insights for vector design and immuno-oncolytic applications. Viruses 2015; 7(11): 6009-42.
[http://dx.doi.org/10.3390/v7112923] [PMID: 26610547]
[37]
Stepanenko AA, Chekhonin VP. Tropism and transduction of oncolytic adenovirus 5 vectors in cancer therapy: focus on fiber chimerism and mosaicism, hexon and pIX. Virus Res 2018; 257: 40-51.
[http://dx.doi.org/10.1016/j.virusres.2018.08.012] [PMID: 30125593]
[38]
Kirn DH, Thorne SH. Targeted and armed oncolytic poxviruses: a novel multi-mechanistic therapeutic class for cancer. Nat Rev Cancer 2009; 9(1): 64-71.
[http://dx.doi.org/10.1038/nrc2545] [PMID: 19104515]
[39]
Kim M. Replicating poxviruses for human cancer therapy. J Microbiol 2015; 53(4): 209-18.
[http://dx.doi.org/10.1007/s12275-015-5041-4] [PMID: 25845536]
[40]
Thorne SH. Immunotherapeutic potential of oncolytic vaccinia virus. Immunol Res 2011; 50(2-3): 286-93.
[http://dx.doi.org/10.1007/s12026-011-8211-4] [PMID: 21717084]
[41]
Parato KA, Breitbach CJ, Le Boeuf F, et al. The oncolytic poxvirus JX-594 selectively replicates in and destroys cancer cells driven by genetic pathways commonly activated in cancers. Mol Ther 2012; 20(4): 749-58.
[http://dx.doi.org/10.1038/mt.2011.276] [PMID: 22186794]
[42]
Moss B. Poxvirus entry and membrane fusion. Virology 2006; 344(1): 48-54.
[http://dx.doi.org/10.1016/j.virol.2005.09.037] [PMID: 16364735]
[43]
Xu R, Johnson AJ, Liggitt D, Bevan MJ. Cellular and humoral immunity against vaccinia virus infection of mice. J Immunol 2004; 172(10): 6265-71.
[http://dx.doi.org/10.4049/jimmunol.172.10.6265] [PMID: 15128815]
[44]
Tang J, Murtadha M, Schnell M, Eisenlohr LC, Hooper J, Flomenberg P. Human T-cell responses to vaccinia virus envelope proteins. J Virol 2006; 80(20): 10010-20.
[http://dx.doi.org/10.1128/JVI.00601-06] [PMID: 17005679]
[45]
Kim JH, Oh JY, Park BH, et al. Systemic armed oncolytic and immunologic therapy for cancer with JX-594, a targeted poxvirus expressing GM-CSF. Mol Ther 2006; 14(3): 361-70.
[http://dx.doi.org/10.1016/j.ymthe.2006.05.008] [PMID: 16905462]
[46]
Tang B, Guo ZS, Bartlett DL, et al. A cautionary note on the selectivity of oncolytic poxviruses. Oncolytic Virother 2019; 8: 3-8.
[http://dx.doi.org/10.2147/OV.S189832] [PMID: 30805315]
[47]
Gulley JL, Arlen PM, Tsang KY, et al. Pilot study of vaccination with recombinant CEA-MUC-1-TRICOM poxviral-based vaccines in patients with metastatic carcinoma. Clin Cancer Res 2008; 14(10): 3060-9.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-0126] [PMID: 18483372]
[48]
Scholl SM, Balloul JM, Le Goc G, et al. Recombinant vaccinia virus encoding human MUC1 and IL2 as immunotherapy in patients with breast cancer. J Immunother 2000; 23(5): 570-80.
[http://dx.doi.org/10.1097/00002371-200009000-00007] [PMID: 11001550]
[49]
Heo J, Reid T, Ruo L, et al. Randomized dose-finding clinical trial of oncolytic immunotherapeutic vaccinia JX-594 in liver cancer. Nat Med 2013; 19(3): 329-36.
[http://dx.doi.org/10.1038/nm.3089] [PMID: 23396206]
[50]
Whitley RJ. Herpes simplex encephalitis: adolescents and adults. Antiviral Res 2006; 71(2-3): 141-8.
[http://dx.doi.org/10.1016/j.antiviral.2006.04.002] [PMID: 16675036]
[51]
Peters C, Rabkin SD. Designing herpes viruses as oncolytics. Mol Ther Oncolytics 2015; 2: 2.
[http://dx.doi.org/10.1038/mto.2015.10] [PMID: 26462293]
[52]
Todo T. Oncolytic virus therapy using genetically engineered herpes simplex viruses. Front Biosci 2008; 13: 2060-4.
[http://dx.doi.org/10.2741/2823] [PMID: 17981691]
[53]
Ning J, Wakimoto H. Oncolytic herpes simplex virus-based strategies: toward a breakthrough in glioblastoma therapy. Front Microbiol 2014; 5: 303.
[http://dx.doi.org/10.3389/fmicb.2014.00303] [PMID: 24999342]
[54]
Tyler KL. Herpes simplex virus infections of the central nervous system: encephalitis and meningitis, including mollaret’s. Herpes 2004; 11(Suppl. 2): a57-64.
[PMID: 15319091]
[55]
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(3): 843-8.
[http://dx.doi.org/10.1073/pnas.94.3.843] [PMID: 9023344]
[56]
Wakimoto H, Kesari S, Farrell CJ, et al. Human glioblastoma-derived cancer stem cells: establishment of invasive glioma models and treatment with oncolytic herpes simplex virus vectors. Cancer Res 2009; 69(8): 3472-81.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-3886] [PMID: 19351838]
[57]
Kanai R, Zaupa C, Sgubin D, et al. Effect of γ34.5 deletions on oncolytic herpes simplex virus activity in brain tumors. J Virol 2012; 86(8): 4420-31.
[http://dx.doi.org/10.1128/JVI.00017-12] [PMID: 22345479]
[58]
Liu BL, Robinson M, Han ZQ, et al. ICP34.5 deleted herpes simplex virus with enhanced oncolytic, immune stimulating, and anti-tumour properties. Gene Ther 2003; 10(4): 292-303.
[http://dx.doi.org/10.1038/sj.gt.3301885] [PMID: 12595888]
[59]
Toda M, Martuza RL, Rabkin SD. Tumor growth inhibition by intratumoral inoculation of defective herpes simplex virus vectors expressing granulocyte-macrophage colony-stimulating factor. Mol Ther 2000; 2(4): 324-9.
[http://dx.doi.org/10.1006/mthe.2000.0130] [PMID: 11020347]
[60]
Maitra R, Ghalib MH, Goel S. Reovirus: a targeted therapeutic-progress and potential. Mol Cancer Res 2012; 10(12): 1514-25.
[http://dx.doi.org/10.1158/1541-7786.MCR-12-0157] [PMID: 23038811]
[61]
Thirukkumaran C, Morris DG. Oncolytic viral therapy using reovirus. Methods Mol Biol 2015; 1317: 187-223.
[http://dx.doi.org/10.1007/978-1-4939-2727-2_12] [PMID: 26072409]
[62]
Thirukkumaran CM, Shi ZQ, Nuovo GJ, et al. Oncolytic immunotherapy and bortezomib synergy improves survival of refractory multiple myeloma in a preclinical model. Blood Adv 2019; 3(5): 797-812.
[http://dx.doi.org/10.1182/bloodadvances.2018025593] [PMID: 30850386]
[63]
Thomis DC, Samuel CE. Mechanism of interferon action: evidence for intermolecular autophosphorylation and autoactivation of the interferon-induced, RNA-dependent protein kinase PKR. J Virol 1993; 67(12): 7695-700.
[PMID: 7693978]
[64]
García MA, Gil J, Ventoso I, et al. Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol Mol Biol Rev 2006; 70(4): 1032-60.
[http://dx.doi.org/10.1128/MMBR.00027-06] [PMID: 17158706]
[65]
Strong JE, Coffey MC, Tang D, Sabinin P, Lee PW. The molecular basis of viral oncolysis: usurpation of the Ras signaling pathway by reovirus. EMBO J 1998; 17(12): 3351-62.
[http://dx.doi.org/10.1093/emboj/17.12.3351] [PMID: 9628872]
[66]
Reuter D, Schneider-Schaulies J. Measles virus infection of the CNS: human disease, animal models, and approaches to therapy. Med Microbiol Immunol (Berl) 2010; 199(3): 261-71.
[http://dx.doi.org/10.1007/s00430-010-0153-2] [PMID: 20390298]
[67]
Schneider-Schaulies J. Meulen Vt, Schneider-Schaulies S. Measles infection of the central nervous system. J Neurovirol 2003; 9(2): 247-52.
[http://dx.doi.org/10.1080/13550280390193993] [PMID: 12707855]
[68]
Iankov ID, Pandey M, Harvey M, Griesmann GE, Federspiel MJ, Russell SJ. Immunoglobulin g antibody-mediated enhancement of measles virus infection can bypass the protective antiviral immune response. J Virol 2006; 80(17): 8530-40.
[http://dx.doi.org/10.1128/JVI.00593-06] [PMID: 16912303]
[69]
Ellerhoff TP, Berchtold S, Venturelli S, et al. Novel epi-virotherapeutic treatment of pancreatic cancer combining the oral histone deacetylase inhibitor resminostat with oncolytic measles vaccine virus. Int J Oncol 2016; 49(5): 1931-44.
[http://dx.doi.org/10.3892/ijo.2016.3675] [PMID: 27601235]
[70]
Shafren DR, Dorahy DJ, Ingham RA, Burns GF, Barry RD. Coxsackievirus A21 binds to decay-accelerating factor but requires intercellular adhesion molecule 1 for cell entry. J Virol 1997; 71(6): 4736-43.
[PMID: 9151867]
[71]
Selinka HC, Wolde A, Sauter M, Kandolf R, Klingel K. Virus-receptor interactions of coxsackie B viruses and their putative influence on cardiotropism. Med Microbiol Immunol (Berl) 2004; 193(2-3): 127-31.
[http://dx.doi.org/10.1007/s00430-003-0193-y] [PMID: 12920584]
[72]
Orthopoulos G, Triantafilou K, Triantafilou M. Coxsackie B viruses use multiple receptors to infect human cardiac cells. J Med Virol 2004; 74(2): 291-9.
[http://dx.doi.org/10.1002/jmv.20184] [PMID: 15332279]
[73]
Shafren DR, Au GG, Nguyen T, et al. Systemic therapy of malignant human melanoma tumors by a common cold-producing enterovirus, coxsackievirus a21. Clin Cancer Res 2004; 10(1 Pt 1): 53-60.
[http://dx.doi.org/10.1158/1078-0432.CCR-0690-3] [PMID: 14734451]
[74]
Bradley S, Jakes AD, Harrington K, Pandha H, Melcher A, Errington-Mais F. Applications of coxsackievirus A21 in oncology. Oncolytic Virother 2014; 3: 47-55.
[http://dx.doi.org/10.2147/OV.S56322] [PMID: 27512662]
[75]
Annels NE, Arif M, Simpson GR, et al. Oncolytic immunotherapy for bladder cancer using coxsackie A21 virus. Mol Ther Oncolytics 2018; 9: 1-12.
[http://dx.doi.org/10.1016/j.omto.2018.02.001] [PMID: 29989024]
[76]
Miyamoto S, Inoue H, Nakamura T, et al. Coxsackievirus B3 is an oncolytic virus with immunostimulatory properties that is active against lung adenocarcinoma. Cancer Res 2012; 72(10): 2609-21.
[http://dx.doi.org/10.1158/0008-5472.CAN-11-3185] [PMID: 22461509]
[77]
Guo ZS, Liu Z, Kowalsky S, et al. Oncolytic immunotherapy: conceptual evolution, current strategies, and future perspectives. Front Immunol 2017; 8: 555.
[http://dx.doi.org/10.3389/fimmu.2017.00555] [PMID: 28555136]
[78]
Angelova AL, Geletneky K, Nüesch JP, Rommelaere J. Tumor selectivity of oncolytic parvoviruses: from in vitro and animal models to cancer patients. Front Bioeng Biotechnol 2015; 3: 55.
[http://dx.doi.org/10.3389/fbioe.2015.00055] [PMID: 25954743]
[79]
Angelova AL, Witzens-Harig M, Galabov AS, Rommelaere J. The oncolytic virotherapy era in cancer management: prospects of applying H-1 parvovirus to treat blood and solid cancers. Front Oncol 2017; 7: 93.
[http://dx.doi.org/10.3389/fonc.2017.00093] [PMID: 28553616]
[80]
Luo Y, Qiu J. Human parvovirus B19: a mechanistic overview of infection and DNA replication. Future Virol 2015; 10(2): 155-67.
[http://dx.doi.org/10.2217/fvl.14.103] [PMID: 26097496]
[81]
Luo Y, Kleiboeker S, Deng X, Qiu J. Human parvovirus B19 infection causes cell cycle arrest of human erythroid progenitors at late S phase that favors viral DNA replication. J Virol 2013; 87(23): 12766-75.
[http://dx.doi.org/10.1128/JVI.02333-13] [PMID: 24049177]
[82]
Rommelaere J, Geletneky K, Angelova AL, et al. Oncolytic parvoviruses as cancer therapeutics. Cytokine Growth Factor Rev 2010; 21(2-3): 185-95.
[http://dx.doi.org/10.1016/j.cytogfr.2010.02.011] [PMID: 20211577]
[83]
Marchini A, Bonifati S, Scott EM, Angelova AL, Rommelaere J. Oncolytic parvoviruses: from basic virology to clinical applications. Virol J 2015; 12: 6.
[http://dx.doi.org/10.1186/s12985-014-0223-y] [PMID: 25630937]
[84]
Geletneky K, Hajda J, Angelova AL, et al. Oncolytic H-1 parvovirus shows safety and signs of immunogenic activity in a first phase I/IIa glioblastoma trial. Mol Ther 2017; 25(12): 2620-34.
[http://dx.doi.org/10.1016/j.ymthe.2017.08.016] [PMID: 28967558]
[85]
Geletneky K, Kiprianova I, Ayache A, et al. Regression of advanced rat and human gliomas by local or systemic treatment with oncolytic parvovirus H-1 in rat models. Neuro-oncol 2010; 12(8): 804-14.
[http://dx.doi.org/10.1093/neuonc/noq023] [PMID: 20299703]
[86]
Kiprianova I, Thomas N, Ayache A, et al. Regression of glioma in rat models by intranasal application of parvovirus h-1. Clin Cancer Res 2011; 17(16): 5333-42.
[http://dx.doi.org/10.1158/1078-0432.CCR-10-3124] [PMID: 21715567]
[87]
Geletneky K, Huesing J, Rommelaere J, et al. Phase I/IIa study of intratumoral/intracerebral or intravenous/intracerebral administration of parvovirus H-1 (ParvOryx) in patients with progressive primary or recurrent glioblastoma multiforme: ParvOryx01 protocol. BMC Cancer 2012; 12: 99.
[http://dx.doi.org/10.1186/1471-2407-12-99] [PMID: 22436661]
[88]
Chiocca EA, Abbed KM, Tatter S, et al. A phase I open-label, dose-escalation, multi-institutional trial of injection with an E1B-Attenuated adenovirus, ONYX-015, into the peritumoral region of recurrent malignant gliomas, in the adjuvant setting. Mol Ther 2004; 10(5): 958-66.
[http://dx.doi.org/10.1016/j.ymthe.2004.07.021] [PMID: 15509513]
[89]
Senac JS, Doronin K, Russell SJ, Jelinek DF, Greipp PR, Barry MA. Infection and killing of multiple myeloma by adenoviruses. Hum Gene Ther 2010; 21(2): 179-90.
[http://dx.doi.org/10.1089/hum.2009.082] [PMID: 19788385]
[90]
Zhang X, Zhao L, Hang Z, Guo H, Zhang M. Evaluation of HSV-1 and adenovirus vector-mediated infection, replication and cytotoxicity in lymphoma cell lines. Oncol Rep 2011; 26(3): 637-44.
[http://dx.doi.org/10.3892/or.2011.1306] [PMID: 21567107]
[91]
Kanai R, Wakimoto H, Cheema T, Rabkin SD. Oncolytic herpes simplex virus vectors and chemotherapy: are combinatorial strategies more effective for cancer? Future Oncol 2010; 6(4): 619-34.
[http://dx.doi.org/10.2217/fon.10.18] [PMID: 20373873]
[92]
Ma W, He H, Wang H. Oncolytic herpes simplex virus and immunotherapy. BMC Immunol 2018; 19(1): 40.
[http://dx.doi.org/10.1186/s12865-018-0281-9] [PMID: 30563466]
[93]
Russell SJ, Peng KW. Measles virus for cancer therapy. Curr Top Microbiol Immunol 2009; 330: 213-41.
[http://dx.doi.org/10.1007/978-3-540-70617-5_11] [PMID: 19203112]
[94]
Msaouel P, Opyrchal M, Domingo Musibay E, Galanis E. Oncolytic measles virus strains as novel anticancer agents. Expert Opin Biol Ther 2013; 13(4): 483-502.
[http://dx.doi.org/10.1517/14712598.2013.749851] [PMID: 23289598]
[95]
Chahlavi A, Todo T, Martuza RL, Rabkin SD. Replication-competent herpes simplex virus vector G207 and cisplatin combination therapy for head and neck squamous cell carcinoma. Neoplasia 1999; 1(2): 162-9.
[http://dx.doi.org/10.1038/sj.neo.7900016] [PMID: 10933051]
[96]
Khuri FR, Nemunaitis J, Ganly I, et al. a controlled trial of intratumoral ONYX-015, a selectively-replicating adenovirus, in combination with cisplatin and 5-fluorouracil in patients with recurrent head and neck cancer. Nat Med 2000; 6(8): 879-85.
[http://dx.doi.org/10.1038/78638] [PMID: 10932224]
[97]
Xia ZJ, Chang JH, Zhang L, 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] Chin J Cancer 2004; 23: 1666-70.
[98]
Stanford MM, Breitbach CJ, Bell JC, McFadden G. Innate immunity, tumor microenvironment and oncolytic virus therapy: friends or foes? Curr Opin Mol Ther 2008; 10(1): 32-7.
[PMID: 18228179]
[99]
Melcher A, Parato K, Rooney CM, Bell JC. Thunder and lightning: immunotherapy and oncolytic viruses collide. Mol Ther 2011; 19(6): 1008-16.
[http://dx.doi.org/10.1038/mt.2011.65] [PMID: 21505424]
[100]
Gujar S, Pol JG, Kim Y, Lee PW, Kroemer G. Antitumor benefits of antiviral immunity: an underappreciated aspect of oncolytic virotherapies. Trends Immunol 2018; 39(3): 209-21.
[http://dx.doi.org/10.1016/j.it.2017.11.006] [PMID: 29275092]
[101]
Zamarin D, Holmgaard RB, Subudhi SK, et al. Localized oncolytic virotherapy overcomes systemic tumor resistance to immune checkpoint blockade immunotherapy. Sci Transl Med 2014; 6(226) 226ra32
[http://dx.doi.org/10.1126/scitranslmed.3008095] [PMID: 24598590]
[102]
Engeland CE, Grossardt C, Veinalde R, et al. CTLA-4 and PD-L1 checkpoint blockade enhances oncolytic measles virus therapy. Mol Ther 2014; 22(11): 1949-59.
[http://dx.doi.org/10.1038/mt.2014.160] [PMID: 25156126]
[103]
Sorensen MR, Holst PJ, Steffensen MA, Christensen JP, Thomsen AR. Adenoviral vaccination combined with CD40 stimulation and CTLA-4 blockage can lead to complete tumor regression in a murine melanoma model. Vaccine 2010; 28(41): 6757-64.
[http://dx.doi.org/10.1016/j.vaccine.2010.07.066] [PMID: 20682365]
[104]
Diaz RM, Galivo F, Kottke T, et al. Oncolytic immunovirotherapy for melanoma using vesicular stomatitis virus. Cancer Res 2007; 67(6): 2840-8.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-3974] [PMID: 17363607]
[105]
Galivo F, Diaz RM, Thanarajasingam U, et al. Interference of CD40L-mediated tumor immunotherapy by oncolytic vesicular stomatitis virus. Hum Gene Ther 2010; 21(4): 439-50.
[http://dx.doi.org/10.1089/hum.2009.143] [PMID: 19922169]
[106]
Wongthida P, Diaz RM, Galivo F, et al. Type III IFN interleukin-28 mediates the antitumor efficacy of oncolytic virus VSV in immune-competent mouse models of cancer. Cancer Res 2010; 70(11): 4539-49.
[http://dx.doi.org/10.1158/0008-5472.CAN-09-4658] [PMID: 20484025]
[107]
Altomonte J, Ebert O. Replicating viral vectors for cancer therapy: strategies to synergize with host immune responses. Microb Biotechnol 2012; 5(2): 251-9.
[http://dx.doi.org/10.1111/j.1751-7915.2011.00296.x] [PMID: 21923638]
[108]
Rajani K, Parrish C, Kottke T, et al. Combination therapy with reovirus and Anti-PD-1 blockade controls tumor growth through innate and adaptive immune responses. Mol Ther 2016; 24(1): 166-74.
[http://dx.doi.org/10.1038/mt.2015.156] [PMID: 26310630]
[109]
Dwyer RM, Khan S, Barry FP, O’Brien T, Kerin MJ. Advances in mesenchymal stem cell-mediated gene therapy for cancer. Stem Cell Res Ther 2010; 1(3): 25.
[http://dx.doi.org/10.1186/scrt25] [PMID: 20699014]
[110]
García-Castro J, Alemany R, Cascalló M, et al. Treatment of metastatic neuroblastoma with systemic oncolytic virotherapy delivered by autologous mesenchymal stem cells: an exploratory study. Cancer Gene Ther 2010; 17(7): 476-83.
[http://dx.doi.org/10.1038/cgt.2010.4] [PMID: 20168350]
[111]
Jain RK, Stylianopoulos T. Delivering nanomedicine to solid tumors. Nat Rev Clin Oncol 2010; 7(11): 653-64.
[http://dx.doi.org/10.1038/nrclinonc.2010.139] [PMID: 20838415]
[112]
Fisher KD, Seymour LW. HPMA copolymers for masking and retargeting of therapeutic viruses. Adv Drug Deliv Rev 2010; 62(2): 240-5.
[http://dx.doi.org/10.1016/j.addr.2009.12.003] [PMID: 20005911]
[113]
Eto Y, Yoshioka Y, Mukai Y, Okada N, Nakagawa S. Development of PEGylated adenovirus vector with targeting ligand. Int J Pharm 2008; 354(1-2): 3-8.
[http://dx.doi.org/10.1016/j.ijpharm.2007.08.025] [PMID: 17904316]
[114]
Duncan R. Polymer conjugates as anticancer nanomedicines. Nat Rev Cancer 2006; 6(9): 688-701.
[http://dx.doi.org/10.1038/nrc1958] [PMID: 16900224]
[115]
Morrison J, Briggs SS, Green N, et al. Virotherapy of ovarian cancer with polymer-cloaked adenovirus retargeted to the epidermal growth factor receptor. Mol Ther 2008; 16(2): 244-51.
[http://dx.doi.org/10.1038/sj.mt.6300363] [PMID: 18071336]
[116]
Choi JW, Lee YS, Yun CO, Kim SW. Polymeric oncolytic adenovirus for cancer gene therapy. J Control Release 2015; 219: 181-91.
[http://dx.doi.org/10.1016/j.jconrel.2015.10.009] [PMID: 26453806]
[117]
Ruf B, Lauer UM. Assessment of current virotherapeutic application schemes: “hit hard and early” versus “killing softly”? Mol Ther Oncolytics 2015; 2: 15018.
[http://dx.doi.org/10.1038/mto.2015.18] [PMID: 27119110]
[118]
Yang L, Pang Y, Moses HL. TGF-beta and immune cells: an important regulatory axis in the tumor microenvironment and progression. Trends Immunol 2010; 31(6): 220-7.
[http://dx.doi.org/10.1016/j.it.2010.04.002] [PMID: 20538542]
[119]
Naik S, Nace R, Federspiel MJ, Barber GN, Peng KW, Russell SJ. Curative one-shot systemic virotherapy in murine myeloma. Leukemia 2012; 26(8): 1870-8.
[http://dx.doi.org/10.1038/leu.2012.70] [PMID: 22425894]
[120]
Durham NM, Mulgrew K, McGlinchey K, et al. Oncolytic VSV primes differential responses to immuno-oncology therapy. Mol Ther 2017; 25(8): 1917-32.
[http://dx.doi.org/10.1016/j.ymthe.2017.05.006] [PMID: 28578991]
[121]
Bishnoi S, Tiwari R, Gupta S, Byrareddy SN, Nayak D. Oncotargeting by vesicular stomatitis virus (VSV): advances in cancer therapy. Viruses 2018; 10(2): 10.
[http://dx.doi.org/10.3390/v10020090] [PMID: 29473868]
[122]
Carew JF, Kooby DA, Halterman MW, Kim SH, Federoff HJ, Fong Y. A novel approach to cancer therapy using an oncolytic herpes virus to package amplicons containing cytokine genes. Mol Ther 2001; 4(3): 250-6.
[http://dx.doi.org/10.1006/mthe.2001.0448] [PMID: 11545616]
[123]
Wang P, Li X, Wang J, et al. Re-designing Interleukin-12 to enhance its safety and potential as an anti-tumor immunotherapeutic agent. Nat Commun 2017; 8(1): 1395.
[http://dx.doi.org/10.1038/s41467-017-01385-8] [PMID: 29123084]
[124]
Edukulla R, Woller N, Mundt B, et al. Antitumoral immune response by recruitment and expansion of dendritic cells in tumors infected with telomerase-dependent oncolytic viruses. Cancer Res 2009; 69(4): 1448-58.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-1160] [PMID: 19190348]
[125]
Lapteva N, Aldrich M, Weksberg D, et al. Targeting the intratumoral dendritic cells by the oncolytic adenoviral vaccine expressing RANTES elicits potent antitumor immunity. J Immunother 2009; 32(2): 145-56.
[http://dx.doi.org/10.1097/CJI.0b013e318193d31e] [PMID: 19238013]
[126]
Samson A, Scott KJ, Taggart D, et al. Intravenous delivery of oncolytic reovirus to brain tumor patients immunologically primes for subsequent checkpoint blockade. Sci Transl Med 2018; 10(422): 10.
[http://dx.doi.org/10.1126/scitranslmed.aam7577] [PMID: 29298869]
[127]
Kleinpeter P, Fend L, Thioudellet C, 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(10) e1220467
[http://dx.doi.org/10.1080/2162402X.2016.1220467] [PMID: 27853644]