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Oncolytic Paramyxoviruses: Mechanism of Action, Preclinical and Clinical Studies

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Abstract

Preclinical studies demonstrate that a broad spectrum of human and animal malignant cells can be killed by oncolytic paramyxoviruses, which includes cells of ecto-, endo- and mesodermal origin. In clinical trials, significant reduction or even complete elimination of primary tumors and established metastases has been reported. Different routes of virus administration (intratumoral, intravenous, intradermal, intraperitoneal, or intrapleural) and single- vs. multiple-dose administration schemes have been explored. The reported side effects were grades 1 and 2, with the most common among them being mild fever. There are certain advantages in using paramyxoviruses as oncolytic agents compared to members of other virus families exist. Thanks to cytoplasmic replication, paramyxoviruses do not integrate the host genome or engage in recombination, which makes them safer and more attractive candidates for widely used therapeutic oncolysis than retroviruses or some DNA viruses. The list of oncolytic Paramyxoviridae members includes the attenuated measles virus, mumps virus, low pathogenic Newcastle disease, and Sendai viruses. Metastatic cancer cells frequently overexpress certain surface molecules that can serve as receptors for oncolytic paramyxoviruses. This promotes specific viral attachment to these malignant cells. Paramyxoviruses are capable of inducing efficient syncytium-mediated lysis of cancer cells and elicit strong immune stimulation, which dramatically enforces anticancer immune surveillance. In general, preclinical studies and phases I–III of clinical trials yield very encouraging results and warrant continued research of oncolytic paramyxoviruses as a particularly valuable addition to the existing panel of cancer-fighting approaches.

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Abbreviations

PFU:

plaque-forming unit

EID50 :

embryo infectious dose 50 (virus dilution that infects 50% of inoculated chicken embryos)

CI:

confidence interval

References

  1. Dock G. 1904. The influence of complicating diseases upon leukemia. Am. J. Med. Sci. 127, 563–592.

    Article  Google Scholar 

  2. De Pace N. 1912. Sulla scomparsa di un enorme cancro vegetante del collo dell’utero senza cura chirurgica. Ginecologia. 9, 82–89.

    Google Scholar 

  3. Levaditi C., Nicolau S. 1923. Vaccine et neoplasmes Ann. Inst. Pasteur. 37, 443–447.

    Google Scholar 

  4. Farber S., Diamond L.K. 1948. Temporary remissions in acute leukemia in children produced by folic acid antagonist, 4-aminopteroyl-glutamic acid. N. Engl. J. Med. 238, 787–793.

    Article  PubMed  CAS  Google Scholar 

  5. Svejda J. 1950. Viruses and tumors. Lek. Listy. 5, 688–689.

    PubMed  CAS  Google Scholar 

  6. Moore A.E. 1954. Effects of viruses on tumors. Annu. Rev. Microbiol. 8, 393–410.

    Article  PubMed  CAS  Google Scholar 

  7. Kelly E., Russell S.J. 2007. History of oncolytic viruses: Genesis to genetic engineering. Mol. Ther. 15, 651–659.

    Article  PubMed  CAS  Google Scholar 

  8. Netesov S.V., Kochneva G.V., Svyatchenko V.A., et al. 2011. Oncolytic viruses: Achievements and problems. Epidemiol. Sanit. (Moscow). 13, 10–17.

    Google Scholar 

  9. Kochneva G.V., Sivolobova G.F., Yudina K.V., et al. 2012. Oncolytic poxviruses. Mol. Genet. Microbiol. Virol. (Moscow). 27 (1), 7–15.

    Article  Google Scholar 

  10. Loktev V.B., Ivankina T.Yu., Netesov S.V., Chumakov P.M. 2012. Oncolytic parvoviruses. New approaches to the treatment of cancer. Bull. Russ. Acad. Med. Sci. 67, 42–47.

    Google Scholar 

  11. Svyatchenko V.A., Tarasova M.V., Netesov S.V., Chumakov P.M. 2012. Oncolytic adenoviruses in anticancer therapy: Current status and prospects. Mol. Biol. (Moscow). 46, 496–507.

    Article  CAS  Google Scholar 

  12. Breitbach C.J., Lichty B.D., Bell J.C. 2016. Oncolytic viruses: Therapeutics with an identity crisis. EBioMedicine. 9, 31–36.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Fukuhara H., Ino Y., Todo T. 2016. Oncolytic virus therapy: A new era of cancer treatment at dawn. Cancer Sci. 107, 1373–1379.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Karapanagiotou E.M., Roulstone V., Twigger K., et al. 2012. Phase I/II trial of carboplatin and paclitaxel chemotherapy in combination with intravenous oncolytic reovirus in patients with advanced malignancies. Clin. Cancer Res. 18, 2080–2089.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Heo J., Reid T., Ruo L., et al. 2013. Randomized dosefinding clinical trial of oncolytic immunotherapeutic vaccinia JX-594 in liver cancer. Nat. Med. 19, 329–336.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Dolgin E. 2015. Oncolytic viruses get a boost with first FDA-approval recommendation. Nat. Rev. Drug Discov. 14, 369–371.

    Article  PubMed  CAS  Google Scholar 

  17. Donina S., Strele I., Proboka G., et al. 2015. Adapted ECHO-7 virus Rigvir immunotherapy (oncolytic virotherapy) prolongs survival in melanoma patients after surgical excision of the tumour in a retrospective study. Melanoma Res. 25, 421–426.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Takaoka A., Hayakawa S., Yanai H., et al. 2003. Integration of interferon-alpha/beta signalling to p53 responses in tumour suppression and antiviral defence. Nature. 424, 516–523.

    Article  PubMed  CAS  Google Scholar 

  19. Tanaka N., Ishihara M., Lamphier M.S., et al. 1996. Cooperation of the tumour suppressors IRF-1 and p53 in response to DNA damage. Nature. 382, 816–818.

    Article  PubMed  CAS  Google Scholar 

  20. Moiseeva O., Mallette F.A., Mukhopadhyay U.K., et al. 2006. DNA damage signaling and p53-dependent senescence after prolonged beta-interferon stimulation. Mol. Biol. Cell. 17, 1583–1592.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Haus O. 2000. The genes of interferons and interferonrelated factors: Localization and relationships with chromosome aberrations in cancer. Arch. Immunol. Ther. Exp. 48, 95–100.

    CAS  Google Scholar 

  22. Mansour M., Palese P., Zamarin D. 2011. Oncolytic specificity of Newcastle disease virus is mediated by selectivity for apoptosis-resistant cells. J. Virol. 85, 6015–6023.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Boisgerault N., Tangy F., Gregoire M. 2010. New perspectives in cancer virotherapy: Bringing the immune system into play. Immunotherapy. 2, 185–199.

    Article  PubMed  CAS  Google Scholar 

  24. Prestwich R.J., Errington F., Diaz R.M., et al. 2009. The case of oncolytic viruses versus the immune system: Waiting on the judgment of Solomon. Hum. Gene Ther. 20, 1119–1132.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Donnelly O.G., Errington-Mais F., Steele L., et al. 2011. Measles virus causes immunogenic cell death in human melanoma. Gene Ther. 20, 7–15.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Bartlett D.L., Liu Z., Sathaiah M., et al. 2013. Oncolytic viruses as therapeutic cancer vaccines. Mol. Cancer. 12, 103.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Yu Y.A., Shabahang S., Timiryasova T.M., et al. 2004. Visualization of tumors and metastases in live animals with bacteria and vaccinia virus encoding light-emitting proteins. Nat. Biotechnol. 22, 313–320.

    Article  PubMed  CAS  Google Scholar 

  28. Lemay C.G., Rintoul J.L., Kus A., et al. 2012. Harnessing oncolytic virus-mediated antitumor immunity in an infected cell vaccine. Mol. Ther. 20, 1791–1799.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Sze D.Y., Reid T.R., Rose S.C. 2013. Oncolytic virotherapy. J. Vasc. Interv. Radiol. 24, 1115–1122.

    Article  PubMed  Google Scholar 

  30. Tai L.H., Zhang J., Scott K.J., et al. 2013. Perioperative influenza vaccination reduces postoperative metastatic disease by reversing surgery-induced dysfunction in natural killer cells. Clin. Cancer Res. 19, 5104–5115.

    Article  PubMed  CAS  Google Scholar 

  31. Matveeva O.V., Guo Z.S., Shabalina S.A., Chumakov P.M. 2015. Oncolysis by paramyxoviruses: multiple mechanisms contribute to therapeutic efficiency. Mol. Ther. Oncolytics. 2, 15011.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Enders G. 1996. Paramyxoviruses. Galveston: Univ. Texas Med. Branch.

    Google Scholar 

  33. Bossart K.N., Fusco D.L., Broder C.C. 2013. Paramyxovirus entry. Adv. Exp. Med. Biol. 790, 95–127.

    Article  PubMed  CAS  Google Scholar 

  34. Matrosovich M., Herrler G., Klenk H.D. 2013. Sialic acid receptors of viruses. Top. Curr. Chem. 7, 73.

    Google Scholar 

  35. Bull C., den Brok M.H., Adema G.J. 2014. Sweet escape: Sialic acids in tumor immune evasion. Biochim. Biophys. Acta. 1846, 238–246.

    PubMed  Google Scholar 

  36. Bull C., Stoel M.A., den Brok M.H., Adema G.J. 2014. Sialic acids sweeten a tumor’s life. Cancer Res. 74, 3199–3204.

    Article  PubMed  CAS  Google Scholar 

  37. Kawaguchi Y., Miyamoto Y., Inoue T., Kaneda Y. 2009. Efficient eradication of hormone-resistant human prostate cancers by inactivated Sendai virus particle. Int. J. Cancer. 124, 2478–2487.

    Article  PubMed  CAS  Google Scholar 

  38. Villar E., Barroso I.M. 2006. Role of sialic acid-containing molecules in paramyxovirus entry into the host cell: a minireview. Glycoconj. J. 23, 5–17.

    Article  PubMed  CAS  Google Scholar 

  39. Anderson B.D., Nakamura T., Russell S.J., Peng K.W. 2004. High CD46 receptor density determines preferential killing of tumor cells by oncolytic measles virus. Cancer Res. 64, 4919–4926.

    Article  PubMed  CAS  Google Scholar 

  40. Surowiak P., Materna V., Maciejczyk A., et al. 2006. CD46 expression is indicative of shorter revival-free survival for ovarian cancer patients. Anticancer Res. 26, 4943–4948.

    PubMed  CAS  Google Scholar 

  41. Maciejczyk A., Szelachowska J., Szynglarewicz B., et al. 2011. CD46 expression is an unfavorable prognostic factor in breast cancer cases. Appl. Immunohistochem. Mol. Morphol. 19, 540–546.

    Article  PubMed  CAS  Google Scholar 

  42. Noyce R.S., Bondre D.G., Ha M.N., et al. 2011. Tumor cell marker PVRL4 (nectin 4) is an epithelial cell receptor for measles virus. PLoS Pathog. 7, e1002240.

    Article  CAS  Google Scholar 

  43. Noyce R.S., Richardson C.D. 2012. Nectin 4 is the epithelial cell receptor for measles virus. Trends Microbiol. 20, 429–439.

    Article  PubMed  CAS  Google Scholar 

  44. Fabre-Lafay S., Garrido-Urbani S., Reymond N., et al. 2005. Nectin-4, a new serological breast cancer marker, is a substrate for tumor necrosis factor-alphaconverting enzyme (TACE)/ADAM-17. J. Biol. Chem. 280, 19543–19550.

    Article  PubMed  CAS  Google Scholar 

  45. Derycke M.S., Pambuccian S.E., Gilks C.B., et al. 2010. Nectin 4 overexpression in ovarian cancer tissues and serum: Potential role as a serum biomarker. Am. J. Clin. Pathol. 134, 835–845.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Takano A., Ishikawa N., Nishino R., et al. 2009. Identification of nectin-4 oncoprotein as a diagnostic and therapeutic target for lung cancer. Cancer Res. 69, 6694–6703.

    Article  PubMed  CAS  Google Scholar 

  47. Myers R., Greiner S., Harvey M., et al. 2005. Oncolytic activities of approved mumps and measles vaccines for therapy of ovarian cancer. Cancer Gene Ther. 12, 593–599.

    Article  PubMed  CAS  Google Scholar 

  48. Fabre-Lafay S., Monville F., Garrido-Urbani S., et al. 2007. Nectin-4 is a new histological and serological tumor associated marker for breast cancer. BMC Cancer. 7, 73.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Kingsbury D.W. 1991. The Paramyxoviruses. New York: Plenum.

    Book  Google Scholar 

  50. Cohen M., Elkabets M., Perlmutter M., et al. 2010. Sialylation of 3-methylcholanthrene-induced fibrosarcoma determines antitumor immune responses during immunoediting. J. Immunol. 185, 5869–5878.

    Article  PubMed  CAS  Google Scholar 

  51. Powell L.D., Whiteheart S.W., Hart G.W. 1987. Cell surface sialic acid influences tumor cell recognition in the mixed lymphocyte reaction. J. Immunol. 139, 262–270.

    PubMed  CAS  Google Scholar 

  52. Galanis E. 2010. Therapeutic potential of oncolytic measles virus: Promises and challenges. Clin. Pharmacol. Ther. 88, 620–625.

    Article  PubMed  CAS  Google Scholar 

  53. Iwata S., Schmidt A.C., Titani K., et al. 1994. Assignment of disulfide bridges in the fusion glycoprotein of Sendai virus. J. Virol. 68, 3200–3206.

    PubMed  PubMed Central  CAS  Google Scholar 

  54. Tashiro M., Yokogoshi Y., Tobita K., et al. 1992. Tryptase Clara, an activating protease for Sendai virus in rat lungs, is involved in pneumopathogenicity. J. Virol. 66, 7211–7216.

    PubMed  PubMed Central  CAS  Google Scholar 

  55. Sakai K., Kohri T., Tashiro M., et al. 1994. Sendai virus infection changes the subcellular localization of tryptase Clara in rat bronchiolar epithelial cells. Eur. Respir. J. 7, 686–692.

    Article  PubMed  CAS  Google Scholar 

  56. Sakai K., Kawaguchi Y., Kishino Y., Kido H. 1993. Electron immunohistochemical localization in rat bronchiolar epithelial cells of tryptase Clara, which determines the pneumotropism and pathogenicity of Sendai virus and influenza virus. J. Hostochem. Cytochem. 41 (1), 89–93.

    Article  CAS  Google Scholar 

  57. Nagai Y. 1995. Virus activation by host proteinases. A pivotal role in the spread of infection, tissue tropism and pathogenicity. Microbiol. Immunol. 39, 1–9.

    PubMed  CAS  Google Scholar 

  58. Kido H., Beppu Y., Sakai K., Towatari T. 1997. Molecular basis of proteolytic activation of Sendai virus infection and the defensive compounds for infection. Biol. Chem. 378, 255–263.

    Article  PubMed  CAS  Google Scholar 

  59. Choi S., Bertram S., Glowacka I., et al. 2009. Type II transmembrane serine proteases in cancer and viral infections. Trends Mol. Med. 15, 303–312.

    Article  PubMed  CAS  Google Scholar 

  60. Abe M., Tahara M., Sakai K., et al. 2013. TMPRSS2 Is an activating protease for respiratory parainfluenza viruses. J. Virol. 87, 11930–11935.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Bertram S., Glowacka I., Blazejewska P., et al. 2010. TMPRSS2 and TMPRSS4 facilitate trypsin-independent spread of influenza virus in Caco-2 cells. J. Virol. 84, 10016–10025.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Bateman A., Bullough F., Murphy S., et al. 2000. Fusogenic membrane glycoproteins as a novel class of genes for the local and immune-mediated control of tumor growth. Cancer Res. 60, 1492–1497.

    PubMed  CAS  Google Scholar 

  63. Bateman A.R., Harrington K.J., Kottke T., et al. 2002. Viral fusogenic membrane glycoproteins kill solid tumor cells by nonapoptotic mechanisms that promote cross presentation of tumor antigens by dendritic cells. Cancer Res. 62, 6566–6578.

    PubMed  CAS  Google Scholar 

  64. Lin E., Salon C., Brambilla E., et al. 2010. Fusogenic membrane glycoproteins induce syncytia formation and death in vitro and in vivo: A potential therapy agent for lung cancer. Cancer Gene Ther. 17, 256–265

    Article  PubMed  CAS  Google Scholar 

  65. Delpeut S., Rudd P.A., Labonte P., von Messling V. 2012. Membrane fusion-mediated autophagy induction enhances morbillivirus cell-to-cell spread. J. Virol. 86, 8527–8535.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Kurooka M., Kaneda Y. 2007. Inactivated Sendai virus particles eradicate tumors by inducing immune responses through blocking regulatory T cells. Cancer Res. 67, 227–236.

    Article  PubMed  CAS  Google Scholar 

  67. Fujihara A., Kurooka M., Miki T., Kaneda Y. 2008. Intratumoral injection of inactivated Sendai virus particles elicits strong antitumor activity by enhancing local CXCL10 expression and systemic NK cell activation. Cancer Immunol. Immunother. 57, 73–84.

    Article  PubMed  Google Scholar 

  68. Senin V., Senina A., Matveeva O. 2014. RF Patent No. 2519763.

    Google Scholar 

  69. Matveeva O.V., Guo Z.S., Senin V.M., et al. 2015. Oncolysis by paramyxoviruses: Preclinical and clinical studies. Mol. Ther. Oncolytics. 2, 15017.

    Article  PubMed Central  CAS  Google Scholar 

  70. Cassel W.A., Murray D.R. 1992. A ten-year follow-up on stage II malignant melanoma patients treated postsurgically with Newcastle disease virus oncolysate. Med. Oncol. Tumor Pharmacother. 9, 169–171.

    PubMed  CAS  Google Scholar 

  71. Batliwalla F.M., Bateman B.A., Serrano D., et al. 1998. A 15-year follow-up of AJCC stage III malignant melanoma patients treated postsurgically with Newcastle disease virus (NDV) oncolysate and determination of alterations in the CD8 T cell repertoire. Mol. Med. 4, 783–794.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Csatary L.K., Eckhardt S., Bukosza I., Czegledi F., Fenyvesi C., Gergely P., Bodey B., Csatary C.M. 1993. Attenuated veterinary virus vaccine for the treatment of cancer. Cancer Detect. Prev. 17, 619–627.

    PubMed  CAS  Google Scholar 

  73. Csatary L.K., Gosztonyi G., Szeberenyi J., Fabian Z., Liszka V., Bodey B., Csatary C.M. 2004. MTH-68/H oncolytic viral treatment in human high-grade gliomas. J. Neurooncol. 67, 83–93.

    Article  PubMed  CAS  Google Scholar 

  74. Freeman A.I., Zakay-Rones Z., Gomori J.M., et al. 2006. Phase I/II trial of intravenous NDV-HUJ oncolytic virus in recurrent glioblastoma multiforme. Mol. Ther. 13, 221–228.

    Article  PubMed  CAS  Google Scholar 

  75. Pecora A.L., Rizvi N., Cohen G.I., et al. 2002. Phase I trial of intravenous administration of PV701, an oncolytic virus, in patients with advanced solid cancers. J. Clin. Oncol. 20, 2251–2266.

    Article  PubMed  CAS  Google Scholar 

  76. Laurie S.A., Bell J.C., Atkins H.L., et al. 2006. A phase 1 clinical study of intravenous administration of PV701, an oncolytic virus, using two-step desensitization. Clin. Cancer Res. 12, 2555–2562.

    Article  PubMed  CAS  Google Scholar 

  77. Lorence R.M., Roberts M.S., O’Neil J.D., et al. 2007. Phase 1 clinical experience using intravenous administration of PV701, an oncolytic Newcastle disease virus. Curr. Cancer Drug Targets. 7, 157–167.

    Article  PubMed  CAS  Google Scholar 

  78. Hotte S.J., Lorence R.M., Hirte H.W., et al. 2007. An optimized clinical regimen for the oncolytic virus PV701. Clin. Cancer Res. 13, 977–985.

    Article  PubMed  CAS  Google Scholar 

  79. Steiner H.H., Bonsanto M.M., Beckhove P., et al. 2004. Antitumor vaccination of patients with glioblastoma multiforme: A pilot study to assess feasibility, safety, and clinical benefit. J. Clin. Oncol. 22, 4272–4281.

    Article  PubMed  Google Scholar 

  80. Karcher J., Dyckhoff G., Beckhove P., et al. 2004. Antitumor vaccination in patients with head and neck squamous cell carcinomas with autologous virusmodified tumor cells. Cancer Res. 64, 8057–8061.

    Article  PubMed  CAS  Google Scholar 

  81. Herold-Mende C., Karcher J., Dyckhoff G., Schirrmacher V. 2005. Antitumor immunization of head and neck squamous cell carcinoma patients with a virusmodified autologous tumor cell vaccine. Adv. Otorhinolaryngol. 62, 173–183.

    PubMed  Google Scholar 

  82. Schulze T., Kemmner W., Weitz J., et al. 2009. 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. 58, 61–69.

    Article  PubMed  CAS  Google Scholar 

  83. Keshelava V.B. 2007. Newcastle disease oncolytic virus and autologous tumor cells in complex cancer therapy. Epidemiol. Vaktsinoprofilakt. 3, 23–28.

    Google Scholar 

  84. Keshelava V.V., Dobrovolskaya N.Y., Podolskaya M.V., Gardarnik T.V. 2009. Organ-preserving treatment of breast cancer with the use of oncolytic Newcastle disease virus. Vestn. Ross. Nauch. Tsentra Rentgenoradiol. 9, 6.

    Google Scholar 

  85. Keshelava V.V., Dobrovolskaya N.Y., Stavitsky R.V., Podolskaya M.V. 2010. Efficacy of the integrated treatment of cervical cancer using the Newcastle disease virus. Radiology–Practice. 15, 38–45.

    Google Scholar 

  86. Heinzerling L., Kunzi V., Oberholzer P.A., et al. 2005. Oncolytic measles virus in cutaneous T-cell lymphomas mounts antitumor immune responses in vivo and targets interferon-resistant tumor cells. Blood. 106, 2287–2294.

    Article  PubMed  CAS  Google Scholar 

  87. Galanis E., Hartmann L.C., Cliby W.A., et al. 2010. Phase I trial of intraperitoneal administration of an oncolytic measles virus strain engineered to express carcinoembryonic antigen for recurrent ovarian cancer. Cancer Res. 70, 875–882.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Russell S.J., Federspiel M.J., Peng K.W., et al. 2014. Remission of disseminated cancer after systemic oncolytic virotherapy. Mayo Clin. Proc. 89, 926–933.

    Article  PubMed  PubMed Central  Google Scholar 

  89. Galanis E., Atherton P.J., Maurer M.J., et al. 2015. Oncolytic measles virus expressing the sodium iodide symporter to treat drug-resistant ovarian cancer. Cancer Res. 75, 22–30.

    Article  PubMed  CAS  Google Scholar 

  90. Asada T. 1974. Treatment of human cancer with mumps virus. Cancer. 34, 1907–1928.

    Article  PubMed  CAS  Google Scholar 

  91. Okuno Y., Asada T., Yamanishi K., et al. 1978. Studies on the use of mumps virus for treatment of human cancer. Biken J. 21, 37–49.

    PubMed  CAS  Google Scholar 

  92. Shimizu Y., Hasumi K., Okudaira Y., et al. 1988. Immunotherapy of advanced gynecologic cancer patients utilizing mumps virus. Cancer Detect. Prev. 12, 487–495.

    PubMed  CAS  Google Scholar 

  93. Emmerson P.T. 1999. Newcastle disease virus (Paramyxoviridae). In: Encyclopedia of Virology. Oxford: Elsevier, pp. 1020–1026.

    Google Scholar 

  94. Swayne D.E., King D.J. 2003. Avian influenza and Newcastle disease. J. Am. Vet. Med. Assoc. 222, 1534–1540.

    Article  PubMed  CAS  Google Scholar 

  95. Flanagan A.D., Love R., Tesar W. 1955. Propagation of Newcastle disease virus in Ehrlich ascites cells in vitro and in vivo. Proc. Soc. Exp. Biol. Med. 90, 82–86.

    Article  PubMed  CAS  Google Scholar 

  96. Lech P.J., Russell S.J. 2010. Use of attenuated paramyxoviruses for cancer therapy. Expert Rev. Vaccines. 9, 1275–1302.

    Article  PubMed  CAS  Google Scholar 

  97. Fournier P., Bian H., Szeberenyi J., Schirrmacher V. 2012. Analysis of three properties of Newcastle disease virus for fighting cancer: Tumor-selective replication, antitumor cytotoxicity, and immunostimulation. Meth. Mol. Biol. 797, 177–204.

    Article  CAS  Google Scholar 

  98. Zamarin D., Palese P. 2012. Oncolytic Newcastle disease virus for cancer therapy: Old challenges and new directions. Future Microbiol. 7, 347–367.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  99. Lam H.Y., Yeap S.K., Rasoli M., et al. 2011. Safety and clinical usage of newcastle disease virus in cancer therapy. J. Biomed. Biotechnol. 718710, 26.

    Google Scholar 

  100. Reichard K.W., Lorence R.M., Cascino C.J., et al. 1992. Newcastle disease virus selectively kills human tumor cells. J. Surg. Res. 52, 448–453.

    Article  PubMed  CAS  Google Scholar 

  101. Fiola C., Peeters B., Fournier P., et al. 2006. Tumor selective replication of Newcastle disease virus: Association with defects of tumor cells in antiviral defence. Int. J. Cancer. 119, 328–338.

    Article  PubMed  CAS  Google Scholar 

  102. Fabian Z., Csatary C.M., Szeberenyi J., Csatary L.K. 2007. p53-independent endoplasmic reticulum stressmediated cytotoxicity of a Newcastle disease virus strain in tumor cell lines. J. Virol. 81, 2817–2830.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  103. Schirrmacher V., Haas C., Bonifer R., et al. 1999. Human tumor cell modification by virus infection: An efficient and safe way to produce cancer vaccine with pleiotropic immune stimulatory properties when using Newcastle disease virus. Gene Ther. 6, 63–73.

    Article  PubMed  CAS  Google Scholar 

  104. Zamarin D., Martinez-Sobrido L., Kelly K., et al. 2009. Enhancement of oncolytic properties of recombinant newcastle disease virus through antagonism of cellular innate immune responses. Mol. Ther. 17, 697–706.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  105. Fabian Z., Torocsik B., Kiss K., et al. 2001. Induction of apoptosis by a Newcastle disease virus vaccine (MTH-68/H) in PC12 rat phaeochromocytoma cells. Anticancer Res. 21, 125–135.

    PubMed  CAS  Google Scholar 

  106. Szeberenyi J., Fabian Z., Torocsik B., et al. 2003. Newcastle disease virus-induced apoptosis in PC12 pheochromocytoma cells. Am. J. Ther. 10, 282–288.

    Article  PubMed  Google Scholar 

  107. Tzadok-David Y., Metzkin-Eizenberg M., Zakay-Rones Z. 1995. The effect of a mesogenic and a lentogenic Newcastle disease virus strain on Burkitt lymphoma Daudi cells. J. Cancer Res. Clin. Oncol. 121, 169–174.

    Article  PubMed  CAS  Google Scholar 

  108. Bar-Eli N., Giloh H., Schlesinger M., Zakay-Rones Z. 1996. Preferential cytotoxic effect of Newcastle disease virus on lymphoma cells. J. Cancer Res. Clin. Oncol. 122, 409–415.

    Article  PubMed  CAS  Google Scholar 

  109. Song K.Y., Wong J., Gonzalez L., et al. 2010. Antitumor efficacy of viral therapy using genetically engineered Newcastle disease virus [NDV(F3aa)-GFP] for peritoneally disseminated gastric cancer. J. Mol. Med. 88, 589–596.

    Article  PubMed  PubMed Central  Google Scholar 

  110. Lorence R.M., Reichard K.W., Katubig B.B., et al. 1994. Complete regression of human neuroblastoma xenografts in athymic mice after local Newcastle disease virus therapy. J. Natl. Cancer Inst. 86, 1228–1233.

    Article  PubMed  CAS  Google Scholar 

  111. Lorence R.M., Katubig B.B., Reichard K.W., et al. 1994. Complete regression of human fibrosarcoma xenografts after local Newcastle disease virus therapy. Cancer Res. 54, 6017–6021.

    PubMed  CAS  Google Scholar 

  112. Phuangsab A., Lorence R.M., Reichard K.W., et al. 2001. Newcastle disease virus therapy of human tumor xenografts: Antitumor effects of local or systemic administration. Cancer Lett. 172, 27–36.

    Article  PubMed  CAS  Google Scholar 

  113. Vigil A., Park M.S., Martinez O., et al. 2007. Use of reverse genetics to enhance the oncolytic properties of Newcastle disease virus. Cancer Res. 67, 8285–8292.

    Article  PubMed  CAS  Google Scholar 

  114. Altomonte J., Marozin S., Schmid R.M., Ebert O. 2010. Engineered newcastle disease virus as an improved oncolytic agent against hepatocellular carcinoma. Mol. Ther. 18, 275–284.

    Article  PubMed  CAS  Google Scholar 

  115. Schirrmacher V., Fournier P. 2009. Newcastle disease virus: A promising vector for viral therapy, immune therapy, and gene therapy of cancer. Meth. Mol. Biol. 542, 565–605.

    Article  CAS  Google Scholar 

  116. Schirrmacher V., Griesbach A., Ahlert T. 2001. Antitumor effects of Newcastle disease virus in vivo: Local versus systemic effects. Int. J. Oncol. 18, 945–952.

    PubMed  CAS  Google Scholar 

  117. Lorence R.M., Pecora A.L., Major P.P., et al. 2003. Overview of phase I studies of intravenous administration of PV701, an oncolytic virus. Curr. Opin. Mol. Ther. 5, 618–624.

    PubMed  CAS  Google Scholar 

  118. Keshelava V.B. 2014. Cancer: Realities and possibilities of application of the Newcastle disease virus. In: Virotherapy: Rationale, Criteria, Indications of Use, Effectiveness. Saarbrücken, Germany: Palmarum Acad.

    Google Scholar 

  119. Keshelava V.B. 2010. Results of a study of the oncolytic Newcastle disease virus in neoadjuvant therapy for breast cancer over a 3-year follow-up period. Vestn. Ross. Nauch. Tsentra Rentgenoradiol. 10, Article ID 04210000150421000022.

    Google Scholar 

  120. Nakamura T., Russell S.J. 2004. Oncolytic measles viruses for cancer therapy. Expert Opin. Biol. Ther. 4, 1685–1692.

    Article  PubMed  CAS  Google Scholar 

  121. Blechacz B., Russell S.J. 2008. Measles virus as an oncolytic vector platform. Curr. Gene Ther. 8, 162–175.

    Article  PubMed  CAS  Google Scholar 

  122. Allen C., Opyrchal M., Aderca I., et al. 2012. Oncolytic measles virus strains have significant antitumor activity against glioma stem cells. Gene Ther. 20, 444–449.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  123. Enders J.F., Katz S.L., Milovanovic M.V., Holloway A. 1960. Studies on an attenuated measles-virus vaccine: 1. Development and preparations of the vaccine: Technics for assay of effects of vaccination. N. Engl. J. Med. 263, 153–159.

    PubMed  CAS  Google Scholar 

  124. Grote D., Russell S.J., Cornu T.I., et al. 2001. Live attenuated measles virus induces regression of human lymphoma xenografts in immunodeficient mice. Blood. 97, 3746–3754.

    Article  PubMed  CAS  Google Scholar 

  125. Dingli D., Peng K.W., Harvey M.E., et al. 2004. Image-guided radiovirotherapy for multiple myeloma using a recombinant measles virus expressing the thyroidal sodium iodide symporter. Blood. 103, 1641–1646.

    Article  PubMed  CAS  Google Scholar 

  126. Studebaker A.W., Kreofsky C.R., Pierson C.R., et al. 2010. Treatment of medulloblastoma with a modified measles virus. Neuro Oncol. 12, 1034–1042.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  127. Phuong L.K., Allen C., Peng K.W., et al. 2003. Use of a vaccine strain of measles virus genetically engineered to produce carcinoembryonic antigen as a novel therapeutic agent against glioblastoma multiforme. Cancer Res. 63, 2462–2469.

    PubMed  CAS  Google Scholar 

  128. Blechacz B., Splinter P.L., Greiner S., et al. 2006. Engineered measles virus as a novel oncolytic viral therapy system for hepatocellular carcinoma. Hepatology. 44, 1465–1477.

    Article  PubMed  CAS  Google Scholar 

  129. Msaouel P., Iankov I.D., Allen C., et al. 2009. Noninvasive imaging and radiovirotherapy of prostate cancer using an oncolytic measles virus expressing the sodium iodide symporter. Mol. Ther. 17, 2041–2048.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  130. McDonald C.J., Erlichman C., Ingle J.N., et al. 2006. A measles virus vaccine strain derivative as a novel oncolytic agent against breast cancer. Breast Cancer Res. Treat. 99, 177–184.

    Article  PubMed  CAS  Google Scholar 

  131. Iankov I.D., Msaouel P., Allen C., et al. 2010. Demonstration of anti-tumor activity of oncolytic measles virus strains in a malignant pleural effusion breast cancer model. Breast Cancer Res. Treat. 122, 745–754.

    Article  PubMed  Google Scholar 

  132. Peng K.W., Hadac E.M., Anderson B.D., et al. 2006. Pharmacokinetics of oncolytic measles virotherapy: Eventual equilibrium between virus and tumor in an ovarian cancer xenograft model. Cancer Gene Ther. 13, 732–738.

    Article  PubMed  CAS  Google Scholar 

  133. Guillerme G., Tangy M., Fonteneau F. 2013. Antitumor virotherapy by attenuated measles virus. Biology. 2, 587–602.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  134. Msaouel P., Dispenzieri A., Galanis E. 2009. Clinical testing of engineered oncolytic measles virus strains in the treatment of cancer: an overview. Curr. Opin. Mol. Ther. 11, 43–53.

    PubMed  PubMed Central  CAS  Google Scholar 

  135. Institute of Laboratory Animal Resources, U.S. Committee on Infectious Diseases of Mice and Rats. 1991. Infectious Diseases of Mice and Rats. Washington, DC: Natl. Acad. Press.

    Google Scholar 

  136. Inoue M., Tokusumi Y., Ban H., et al. 2003. A new Sendai virus vector deficient in the matrix gene does not form virus particles and shows extensive cell-tocell spreading. J. Virol. 77, 6419–6429.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  137. Yonemitsu Y., Ueda Y., Kinoh H., Hasegawa M. 2008. Immunostimulatory virotherapy using recombinant Sendai virus as a new cancer therapeutic regimen. Front. Biosci. 13, 1892–1898.

    Article  PubMed  CAS  Google Scholar 

  138. Iwadate Y., Inoue M., Saegusa T., et al. 2005. Recombinant Sendai virus vector induces complete remission of established brain tumors through efficient interleukin-2 gene transfer in vaccinated rats. Clin. Cancer Res. 11, 3821–3827.

    Article  PubMed  CAS  Google Scholar 

  139. Matveeva O.V., Kochneva G.V., Netesov S.V. et al. 2015. Mechanisms of oncolysis by paramyxovirus Sendai. Acta Naturae 7 (2), 6–17.

    PubMed  PubMed Central  CAS  Google Scholar 

  140. Tanemura A., Kiyohara E., Katayama I., Kaneda Y. 2013. Recent advances and developments in the antitumor effect of the HVJ envelope vector on malignant melanoma: from the bench to clinical application. Cancer Gene Ther. 20, 599–605.

    Article  PubMed  CAS  Google Scholar 

  141. Slobod K.S., Shenep J.L., Lujan-Zilbermann J., et al. 2004. Safety and immunogenicity of intranasal murine parainfluenza virus type 1 (Sendai virus) in healthy human adults. Vaccine. 22, 3182–3186.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Biopolymer Design LLC, Acton, Massachusetts, United States

    O. V. Matveeva

  2. State Research Center of Virology and Biotechnology Vector, Koltsovo, Novosibirsk oblast, 630559, Russia

    G. V. Kochneva & S. S. Zainutdinov

  3. Novosibirsk State University, Novosibirsk, 630090, Russia

    G. V. Kochneva & S. S. Zainutdinov

  4. Russian Research Center of Medical Rehabilitation and Balneology, Moscow, 121099, Russia

    G. V. Ilyinskaya

  5. Blokhin Cancer Research Center, Moscow, 115478, Russia

    G. V. Ilyinskaya

  6. Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, Moscow, 119991, Russia

    P. M. Chumakov

  7. Chumakov Federal Scientific Center for Research and Development of Immune and Biological Products, Russian Academy of Sciences, Moscow, 108819, Russia

    P. M. Chumakov

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  1. O. V. Matveeva
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Correspondence to O. V. Matveeva.

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Original Russian Text © O.V. Matveeva, G.V. Kochneva, S.S. Zainutdinov, G.V. Ilyinskaya, P.M. Chumakov, 2018, published in Molekulyarnaya Biologiya, 2018, Vol. 52, No. 3, pp. 360–379.

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Matveeva, O.V., Kochneva, G.V., Zainutdinov, S.S. et al. Oncolytic Paramyxoviruses: Mechanism of Action, Preclinical and Clinical Studies. Mol Biol 52, 306–322 (2018). https://doi.org/10.1134/S002689331803010X

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