Immunobiology of Anticancer Virotherapy With Newcastle Disease Virus in Cancer Patients
DOI:
https://doi.org/10.17140/VROJ-2-108Keywords:
Virotherapy, Newcastle disease virus (NDV), Cancer treatment, Antitumor immune responses, ApoptosisAbstract
Virotherapy with oncolytic viruses that preferentially infect and kill cancer cells is a novel and promising strategy for cancer treatment. Newcastle disease virus( NDV), which is pathogenic in birds, has beneficial clinical effects in cancer patients. NDV virotherapy is safe and elicits an antitumor response in patients affected by different types of cancers. The selective replication of NDV in tumor cells, the lack of genetic recombination, the lack of interaction with host cell DNA, and safety of NDV vaccination in cancer patients has resulted in NDV virotherapy to be accepted as a potentially attractive anticancer modality. However, more knowledge is needed to support the development of optimal NDV-based treatment modality for cancer. In this paper, the biological characteristics of NDV, the clinical effectiveness of NDV-based anticancer vaccination, immunobiology of NDV virotherapy in cancer patients, immune responses to NDV vaccines, and NDV-induced immunogenic cell death and apoptosis of cancer cells have been discussed in detail.
References
Fukuhara H, Ino Y, Todo T. Oncolytic virus therapy: A new era of cancer treatment at dawn. Cancer Sci. 2016; 107(10): 1373-1379. doi: 10.1111/cas.13027
Lawler SE, Speranza MC, Cho CF, Chiocca EA. Oncolytic viruses in cancer treatment: A review. JAMA Oncol. 2017; 3(6): 841-849. doi: 10.1001/jamaoncol.2016.2064
Bonab SF, Khansari N. Virotherapy with newcastle disease virus for cancer treatment and its efficacy in clinical trials. MOJ Immunol. 2017; 5(6): 00176. doi: 10.15406/moji.2017.05.00176
Sinkovics J. Enhancement of carcinostatic activity of Newcastle disease virus (NDV) associated with adaptation to suckling mouse brain. Bacteriol Proc. 1957; 96: M108.
Cassel WA, Garrett RE. Newcastle disease virus as an an-tineoplastic agent. Cancer. 1965; 18(7): 863-868. doi: 10.1002/1097-0142(196507)18:7<863::AID-CNCR28201807 14>3.0.CO;2-V
Cassel WA, Garrett RE. Tumor immunity after viral oncolysis. J Bacteriol. 1966; 92(3): 792.
Heicappell R, Schirrmacher V, von Hoegen P, Ahlert T, Appelhans B. Prevention of metastatic spread by postoperative immunotherapy with virally modified autologous tumor cells. I. Parameters for optimal therapeutic effects. Int J Cancer. 1986;37(4): 569-577. doi: 10.1002/ijc.2910370416
Czegledi A, Ujvari D, Somogyi E, et al. Third genome size category of avian paramyxovirus serotype 1 (Newcastle disease virus) and evolutionary implications. Virus Res. 2006; 120(1-2): 36-48. doi: 10.1016/j.virusres.2005.11.009
Lamb RA, Parks GD. Paramyxoviridae: Their viruses and their replication. In: Fields BN, Knipe DM, Howley PM, eds. Fields Virology. 5th ed. Philadelphia, PA, USA: Wolters Kluwer and Lippincot Williams and Willkins; 2007.
MacLachlan NJ, Dubovi EJ. Paramyxoviridae and pneumo-viridae. In: Fenner’s Veterinary Virology. 5th ed. San Diego, CA, USA: Academic Press; 2016: 327-356.
Huang Z, Krishnamurthy S, Panda A, Samal SK. Newcastle disease virus V protein is associated with viral pathogenesis and functions as an alphainterferon antagonist. J Virol. 2003; 77: 8676-8685. doi: 10.1128/JVI.77.16.8676-8685.2003
Park MS, Garcia-SastreA, Cros JF, Basler CF, Palese P. Newcastle disease virus V protein is a determinant of host-range restriction. J Virol. 2003; 77(17): 9522-9532. doi: 10.1128/ JVI.77.17.9522-9532.2003
Janke M, Peeters B, de Leeuw O, et al. Recombinant Newcastle disease virus (NDV) with inserted gene coding for GM-CSF as a new vector for cancer immunogene therapy. Gene Ther. 2007; 14(23): 1639-1649. doi: 10.1038/sj.gt.3303026
Miller PJ, Koch G. Newcastle disease. In: Swayne DE, Glisson JR, McDougald LR, Nolan LK, Suarez DL, Nair VL, eds. Diseases of Poultry. 13th ed. Hoboken, NJ, USA: Wiley-Blackwell. 2013: 89-138.
Reichard KW, Lorence RM, Cascino CJ, et al. Newcastle disease virus selectively kills human tumor cells. J Surg Res. 1992; 52(5): 448-453. doi: 10.1016/0022-4804(92)90310-V
Walter RJ, Attar BM, Rafiq A, Tejaswi S, Delimata M. Newcastle disease virus LaSota strain kills human pancreatic cancer cells in vitro with high selectivity. JOP. 2012; 13(1): 45- 53.
Silberhumer GR, Brader P, Wong J, et al. Genetically engineered oncolytic Newcastle disease virus effectively induces sustained remission of malignant pleural mesothelioma. Mol Cancer Ther. 2010; 9(10): 2761-2769. doi: 10.1158/1535-7163. MCT-10-0090
Schirrmacher V. Oncolytic Newcastle disease virus as a prospective anti-cancer therapy. A biologic agent with potential to break therapy resistance. Exp Opin Biol Ther. 2015; 15(12): 1757-1771. doi: 10.1517/14712598.2015.1088000
Ch’ng WC, Stanbridge EJ, Yusoff K, Shafee N. The oncolytic activity of Newcastle disease virus in clear cell carcinoma cells in normoxic and hypoxic conditions: The interplay between VHL and interferon-β signaling. J Interferon Cytokine Res. 2013; 33(7): 346-354. doi: 10.1089/jir.2012.0095
Fiola C, Peeters B, Fournier P, et al. Tumor selective replication of Newcastle disease virus: Association with defects of tumor cells in antiviral defence. Int J Cancer. 2006; 119(2): 328-338. doi: 10.1002/ijc.21821
Krishnamurthy S, Takimoto T, Scroggs RA, Portner A. Differentially regulated interferon response determines the outcome of Newcastle disease virus infection in normal and tumor cell lines. J Virol. 2006; 80(11): 5145-5155. doi: 10.1128/ JVI.02618-05
Wilden H, Fournier P, Zawatzky R, Schirrmacher V. Expres-sion of RIG-I, IRF3, IFN-β and IRF7 determines resistance or susceptibility of cells to infection by Newcastle disease virus. Int J Oncol. 2009; 34(4): 971-982. doi: 10.3892/ijo_00000223
Puhlmann J, Puehler F, Mumberg D, Boukamp P, Beier R. Rac 1 is required for oncolytic NDV replication in human cancer cells and establishes a link between tumorigenesis and sensitivity to oncolytic virus. Oncogene. 2010; 29(15): 2205- 2216. doi: 10.1038/onc.2009.507
Elankumaran S, Chavan V, Qiao D, et al. Type I interferon-sensitive recombinant newcastle disease virus for oncolytic virotherapy. J Virol. 2010; 84(8): 3835-3844. doi: 10.1128/ JVI.01553-09
Buijs PR, van Eijck CH, Hofland LJ, Fouchier RA, van den Hoogen BG. Different responses of human pancreatic adenocarcinoma cell lines to oncolytic Newcastle disease virus infection. Cancer Gen Ther. 2014; 21(1): 24-30. doi: 10.1038/ cgt.2013.78
Biswas M, Kumar SR,Allen A, et al. Cell-type-specific innate immune response to oncolytic Newcastle disease virus. Viral immunol. 2012; 25(4): 268-276. doi: 10.1089/vim.2012.0020
Mansour M, Palese P, Zamarin D. Oncolytic specificity of Newcastle disease virus is mediated by selectively for apoptosis-resistant cells. J Virol. 2011; 85: 6015-6023. doi: 10.1128/ JVI.01537-10
Csatary LK, Eckhard S, Bukosza I, et al. Attenuated veterinary virus vaccine for the treatment of cancer. Cancer Detect Prev. 1993; 17(6): 619-627.
Csatary LK, Gosztonyi G, Szeberenyi J, et al. MTH-68/H oncolytic viral treatment in human high-grade gliomas. J Neuro Oncol. 2004; 67(1-2): 83-93. doi: 10.1023/B:NE ON.0000021735.85511.05
Pecora AL, Rizvi N, Cohen GI, et al. Phase I trial of intravenous administration of PV701, an oncolytic virus, in patients with advanced solid cancers. J Clin Oncol. 2002; 20(9): 2251-2266. doi: 10.1038/mt.2016.101
Liang W, Wang H, Sun TM, et al. Application of autologous tumor cell vaccine and NDV vaccine in treatment of tumors of digestive tract. World J Gastroenterol. 2003; 9(3): 495-498. doi: 10.3748/wjg.v9.i3.495
Lorence RM, Roberts MS, O’Neil JD, et al. Phase 1 clinical experience using intravenous administration of PV701, an oncolytic Newcastle disease virus. Curr Cancer Drug Targets. 2007; 7(2): 157-167. doi: 10.2174/156800907780058853
Cassel WA, Murray DR. A ten-year follow-up on stage II malignant melanoma patients treated postsurgically with Newcastle disease virus oncolysate. Med Oncol Tumor Pharmacother. 1992; 9(4): 169-171. doi: 10.1007/BF02987752
Voit C, Kron M, Schwurzer-Voit M, Sterry W. Intradermal injection of Newcastle disease virus-modified autologous melanoma cell lysate and interleukin-2 for adjuvant treatment of melanoma patients with resectable stage III disease. J Dtsch Dermatol Ges. 2003; 1(2): 120-125. doi: 10.1046/j.1610- 0387.2003.02014.x
Ockert D, Schirrmacher V, Beck N, et al. Newcastle disease virus-infected intact autologous tumor cell vaccine for adjuvant active specific immunotherapy of resected colorectal carcinoma. Clin Cancer Res. 1996; 2(1): 21-28.
Schulze T, Kemmner W, Weitz J, et al. Efficiency of adjuvant active specific immunization with Newcastle disease virus modified tumor cells in colorectal cancer patients following resection of liver metastases: Results of a prospective randomized trial. Cancer Immunol Immunother. 2009; 58(1): 61-69. doi: 10.1007/s00262-008-0526-1
Schirrmacher V, Bihari AS, Stuecker W, Sprenger T. Long-term remission of prostate cancer with extensive bone metastases upon immuno- and virotherapy: A case report. Oncol Lett. 2014; 8(6): 2403-2406.
Schirrmacher V, Stuecker W, Lulei M, Bihari AS, Sprenger T. Long-term survival of a breast cancer patient with extensive liver metastases upon immune and virotherapy: A case report. Immunotherapy. 2015; 7(8): 855-860. doi: 10.3892/ol.2014.2588
Freeman AI, Zakay-Rones Z, Gomori JM, et al. Phase I/ II trial of intravenous NDV-HUJ oncolytic virus in recurrent glioblastoma multiforme. Mol Ther. 2006; 13(1): 221-228. doi: 10.1016/j.ymthe.2005.08.016
Liebrich W, Schlag P, Manasterski M, et al. In vitro and clinical characterisation of a Newcastle disease virus-modified autologous tumourcell vaccine for treatment of colorectal cancer patients. Eur J cancer. 1991; 27(6): 703-710. doi: 10.1016/0277-5379(91)90170-I
Bohle W, Schlag P, Liebrich W, et al. Postoperative active specific immunization in colorectal cancer patients with virus-modified autologous tumor-cell vaccine. First clinical results with tumor-cell vaccines modified with live but avirulent Newcastle disease virus. Cancer. 1990; 66(7): 1517- 1523. doi: 10.1002/1097-0142(19901001)66:7<1517::AID-CNCR2820660714>3.0.CO;2-I
Steiner HH, Bonsanto MM, Beckhove P, et al. Antitumor vaccination of patients with glioblastoma multiforme: A pilot study to assess feasibility, safety, and clinical benefit. J Clin Oncol. 2004; 22(21): 4272-4281. doi: 10.1200/JCO.2004.09.038
Karcher J, Dyckhoff G, Beckhove P, et al. Antitumor vaccination in patients with head and neck squamous cell carcinomas with autologous virus-modified tumor cells. Cancer Res. 2004; 64(21): 8057-8061. doi: 10.1158/0008-5472.CAN-04-1545
Herold-Mende C, Karcher J, Dyckhoff G, Schirrmacher V. Antitumor immunization of head and neck squamous cell carcinoma patients with a virus-modified autologous tumor cell vaccine. Adv Otorhinolaryngol. 2005; 62: 173-183. doi: 10.1159/000082507
Pomer S, Schirrmacher V, Thiele R, et al. Tumor response and 4 year survival-data of patients with advanced renal-cell carcinoma treated with autologous tumor vaccine and sucutaneous R-IL-2 and IFN-α(2b). Int J Oncol. 1995; 6(5): 947-954. doi: 10.3892/ijo.6.5.947
Molouki A, Peeters B. Rescue of recombinant Newcastle disease virus: Current cloning strategies and RNA polymerase provision systems. Arch Virol. 2017; 162(1): 1-12. doi: doi: 10.1007/s00705-016-3065-7
Molouki A, Peeters B. Rescue of recombinant Newcastle disease virus: A short history of how it all started. Arch Virol. 2017; 162(7): 1845-1854. doi: 10.1007/s00705-017-3308-2
Wu Y, He J, An Y, et al. Recombinant Newcastle disease vi-rus (NDV/Anh-IL-2) expressing human IL-2 as a potential can-didate for suppresses growth of hepatoma therapy. J Pharma-col Sci. 2016; 132(1): 24-30. doi: 10.1016/j.jphs.2016.03.012
Wu Y, He J, Geng J, et al. Recombinant Newcastle disease vi-rus expressing human TRAIL as a potential candidate for hepato-ma therapy. Eur J Pharmacol. 2017; 802: 85-92. doi: 10.1016/j. ejphar.2017.02.042
Xu X, Sun Q, Yu X, Zhao L. Rescue of nonlytic new-castle disease virus (NDV) expressing IL-15 for cancerim-munotherapy. Virus Res. 2017; 233: 35-41. doi: 10.1016/j.vi-rusres.2017.03.003
Schirrmacher V, Bihari AS, Stuecker W, Sprenger T. Long-term remission of prostate cancer with extensive bone metasta-ses upon immuno- and virotherapy: A case report. Oncol Lett. 2014; 8(6): 2403-2406. doi: 10.3892/ol.2014.2588
Schirrmacher V, Stuecker W, Lulei M, Bihari AS, Sprenger T. Long-term survival of a breast cancer patient with extensive liver metastases upon immune and virotherapy: A case report. Immunotherapy. 2014; 7(8): 855-860. doi: 10.2217/imt.15.48
Ockert D, Schirrmacher V, Beck N, Stoelben E, Ahlert T. Newcastle disease virus-infected intact autologous tumor cell vaccine for adjuvant active specific immunotherapy of resected colorectal carcinoma. Clin Cancer Res. 1996; 2: 21-28
Schirrmacher V, Heicappell R. Prevention of metastatic spread by postoperative immunotherapy with virally modified autologous tumor cells. II. Establishment of specific systemic anti-tumor immunity. Clin Exp Metastasis. 1987; 5(2): 147-156. doi: 10.1007/BF00058060
Von Hoegen P, Weber E, Schirrmacher V. Modification of tumor cells by a low dose of Newcastle disease virus: Augmentation of the tumor-specific T cell response in the absence of an anti-viral response. Eur J Immunol. 1988; 18: 1159-1166. doi: 10.1002/eji.1830180803
Von Hoegen P, Zawatzky R, Schirrmacher V. Modification of tumor cells by a low dose of Newcastle disease virus. III. Potentiation of tumor specific cytolytic T cell activity via induction of interferon-alpha/beta. Cell Immunol. 1990; 126: 80-90. doi: 10.1016/0008-8749(90)90302-8
Termeer CC, Schirrmacher V, Bröcke EB, Becker JC. Newcastle disease virus infection induces B7-1/B7-2- independent T-cell costimulatory activity in human melanoma cells. Cancer Gene Ther. 2000;7: 316-323.
Schild H, von Hoegen P, Schirrmacher V. Modification of tumor cells by a low dose of Newcastle disease virus. II. Augmented tumor-specific T cell response as a result of CD4+ and CD8+ immune T cell cooperation. Cancer Immunol Immunother. 1989; 28(1): 22-28. doi: 10.1007/BF00205796
Schirrmacher V, Haas C, Bonifer R, Ertel C. Virus potentiation of tumor vaccine T-cell stimulatory capacity requires cell surface binding but not infection. Clin Cancer Res. 1997; 3(7): 1135- 1148.
Koks CA, Garg AD, Ehrhardt M, et al. Newcastle disease virotherapy induces long-term survival and tumor-specific immune memory in ortheotopicglioma through the induction of immunogenic cell death. Int J Cancer. 2015; 136(5): E313-E325. doi: 10.1002/ijc.29202
Ertel C, Millar NS, Emmerson PT, Schirrmacher V, von Hoe-gen P. Viral hemagglutinin augments peptide-specific cytotoxic T cell responses. Eur J Immunol. 1993, 23(10): 2592-2596. doi: 10.1002/eji.1830231032
Jurianz K, Haas C, Hubbe M, et al. Adhesive function of Newcastle disease virus hemagglutinin in tumor–host interac-tion. Int J Oncol. 1995; 7(3): 539-545.
Schirrmacher V, Schlude C, Weitz J, Beckhove P. Strong T-cell costimulation can reactivate tumor antigen-specific T cells in late-stage metastasized colorectal carcinoma patients: Results from a phase I clinical study. Int J Oncol. 2015; 46(1): 71-77. doi: 10.3892/ijo.2014.2692
Ni J, Galani IE, Cerwenka A, Schirrmacher V, Fournier P. Antitumor vaccination by Newcastle disease virus hemaggluti-nin-neuraminidase plasmid DNA application: Changes in tumor microenvironment and activation of innate anti-tumor immu-nity. Vaccine. 2011; 29: 1185-1193. doi: doi: 10.1016/j.vac-cine.2010.12.005
Zamarin D, Holmgaard RB, Subudhi SK, et al. Local-ized oncolytic virotherapy overcomes systemic tumor resis-tance to immune checkpoint blockade immunotherapy. Sci Transl Med. 2014; 6(226): 226ra232. doi: 10.1016/j.vac-cine.2010.12.005
Lorence RM, Katubig BB, Reichard KW, et al. Complete re-gression of human fibrosarcoma xenografts after local Newcas-tle disease virus therapy. Cancer Res. 1994; 54(23): 6017-6021.
Jarahian M, Watzl C, Fournier P, et al. Activation of natural killer cells by Newcastle disease virus hemagglutinin-neuramin-idase. J Virol. 2009; 83: 8108-8121. doi: 10.1128/JVI.00211-09
Umansky V, Shatrov VA, Lehmann V, Schirrmacher V. Induction of NO synthesis in macrophages by Newcastle disease virus is associated with activation of nuclear factor-kappa B. Int Immunol. 1996; 8(4): 491-398.
Washburn B, Weigand MA, Grosse-Wilde A, et al. TNF-related apoptosis-inducing ligand mediates tumoricidal activity of human monocytes stimulated by Newcastle disease virus. J Immunol. 2003; 170(4): 1814-1821. doi: 10.4049/jimmu-nol.170.4.1814
Zeng J, Fournier P, Schirrmacher V. Induction of interferon-αand tumor necrosis factor-related apoptosis-inducing ligand in human blood mononuclear cells by hemaggluzinin-neuramin-idase but not F protein of Newcastle disease virus. Virology. 2002; 297(1): 19-30. doi: 10.1006/viro.2002.1413
Schirrmacher V, Bai L, Umansky V, Yu L, Xing Y, Qian Z. Newcastle disease virus activates macrophages for anti-tu-mor activity. Int J Oncol. 2000; 16(2): 363-373. doi: 10.3892/ ijo.16.2.363
Kawai T, Akira S. Toll-like receptor and RIG-I-like receptor signaling. Ann NY Acad Sci. 2008; 1143: 1-20. doi: 10.1196/ annals.1443.020
Fournier P, Wilden H, Schirrmacher V. Importance of retinoic-acid-inducible gene I and of receptor for type I interferon for cellular resistance to infection by Newcastle disease virus. Int J Oncol. 2012; 40: 287-298. doi: 10.3892/ijo.2011.1222
Fournier P, Arnold A, Schirrmacher V. Polarization of human monocyte-derived dendritic cells to DC1 by in vitro stimulation with Newcastle disease virus. J BUON. 2009; 14(Suppl 1): S111-S122.
Bai L, Koopmann J, Fiola C, Fournier P, Schirrmacher V. Dendritic cells pulsed with viral oncolysate potently stimulate autologous T cells from cancer patients. Int J Oncol. 2002; 21: 685-694. doi: 10.3892/ijo.21.4.685
Wie D, Sun N, Nan G, et al. Construction of recombinant Newcastle disease virus Italien strain for oncolytic virotherapy of tumors. Hum Gene Ther. 2012; 23(7): 700-710. doi: 10.1089/ hum.2011.207
Washburn B, Schirrmacher V. Human tumor cell infection by Newcastle Disease Virus leads to upregulation of HLA and cell adhesion molecules and to induction of interferons, chemokines and finally apoptosis. Int J Oncol. 2002; 21: 85-93. doi: 10.3892/ ijo.21.1.85
Ahmad U, AhmedI, Keong YY, AbdManan N, Othman F. Inhibitory and apoptosis-inducing effects of Newcastle dis-ease virus strain AF2240 on mammary carcinoma cell line. Biomed Res Int. 2015; 2015: 127828. doi: 10.1155/2015/127828
Elankumaran, S, Rockemann D, Samal SK. Newcastle dis-ease virus exerts oncolysis by both intrinsic and extrinsic cas-pase-dependent pathways of cell death. J Virol. 2006; 80(15): 7522-7534. doi: 10.1128/JVI.00241-06
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