Antitumor virotherapy consists of the use of replication-competent viruses to infect and kill tumor cells preferentially, without damaging healthy cells. Vaccine-attenuated strains of measles virus (MV) are good candidates for this approach. Attenuated MV uses the CD46 molecule as a major entry receptor into cells. This molecule negatively regulates the complement system and is frequently overexpressed by cancer cells to escape lysis by the complement system. MV exhibits oncolytic properties in many cancer types in vitro, and in mouse models. Phase I clinical trials using MV are currently underway. Here, we review the state of this therapeutic approach, with a focus on the effects of MV on the antitumor immune response.
References
[1]
Boisgerault, N.; Tangy, F.; Gregoire, M. New perspectives in cancer virotherapy: Bringing the immune system into play. Immunotherapy 2010, 2, 185–199, doi:10.2217/imt.10.6.
Nomenclature for describing the genetic characteristics of wild-type measles viruses (update). Wkly. Epidemiol. Rec. 2001, 76, 249–251.
[11]
Enders, J.F.; Peebles, T.C. Propagation in tissue cultures of cytopathogenic agents from patients with measles. Proc. Soc. Exp. Biol. Med. 1954, 86, 277–286.
[12]
Bankamp, B.; Takeda, M.; Zhang, Y.; Xu, W.; Rota, P.A. Genetic characterization of measles vaccine strains. J. Infect. Dis. 2011, 204, S533–S548, doi:10.1093/infdis/jir097.
[13]
Schwarz, A.J. Preliminary tests of a highly attenuated measles vaccine. Am. J. Dis. Child. 1962, 103, 386–389.
World Health Organisation: Immunization, Vaccines and Biologicals: Measles. Available online: http://www.who.int/immunization/topics/measles/en/index.html/ (accessed on 24 April 2012).
[16]
Griffin, D. Measles virus. In Field’s Virology; Knipe, D., Howley, P., Eds.; Lippincott-Raven Publishers: Philadelphia, PA, USA, 2001; Volume 2, pp. 1401–1441.
[17]
Lievano, F.; Galea, S.A.; Thornton, M.; Wiedmann, R.T.; Manoff, S.B.; Tran, T.N.; Amin, M.A.; Seminack, M.M.; Vagie, K.A.; Dana, A.; et al. Measles, mumps, and rubella virus vaccine (m-m-rii): A review of 32 years of clinical and postmarketing experience. Vaccine 2012, 30, 6918–6926, doi:10.1016/j.vaccine.2012.08.057.
[18]
Parker Fiebelkorn, A.; Redd, S.B.; Gallagher, K.; Rota, P.A.; Rota, J.; Bellini, W.; Seward, J. Measles in the united states during the postelimination era. J. Infect. Dis. 2010, 202, 1520–1528, doi:10.1086/656914.
[19]
Progress towards measles elimination in who’s european region, 2005–2008. Wkly. Epidemiol. Rec. 2009, 84, 57–64.
[20]
Wolfson, L.J.; Strebel, P.M.; Gacic-Dobo, M.; Hoekstra, E.J.; McFarland, J.W.; Hersh, B.S. Has the 2005 measles mortality reduction goal been achieved? A natural history modelling study. Lancet 2007, 369, 191–200.
[21]
Hilleman, M.R. Current overview of the pathogenesis and prophylaxis of measles with focus on practical implications. Vaccine 2001, 20, 651–665, doi:10.1016/S0264-410X(01)00384-X.
[22]
Hsu, E.C.; Iorio, C.; Sarangi, F.; Khine, A.A.; Richardson, C.D. Cdw150(slam) is a receptor for a lymphotropic strain of measles virus and may account for the immunosuppressive properties of this virus. Virology 2001, 279, 9–21, doi:10.1006/viro.2000.0711.
[23]
Tatsuo, H.; Ono, N.; Tanaka, K.; Yanagi, Y. Slam (cdw150) is a cellular receptor for measles virus. Nature 2000, 406, 893–897.
[24]
Anderson, B.D.; Nakamura, T.; Russell, S.J.; Peng, K.W. High cd46 receptor density determines preferential killing of tumor cells by oncolytic measles virus. Cancer Res. 2004, 64, 4919–4926, doi:10.1158/0008-5472.CAN-04-0884.
[25]
Dorig, R.E.; Marcil, A.; Chopra, A.; Richardson, C.D. The human cd46 molecule is a receptor for measles virus (edmonston strain). Cell 1993, 75, 295–305, doi:10.1016/0092-8674(93)80071-L.
[26]
Naniche, D.; Varior-Krishnan, G.; Cervoni, F.; Wild, T.F.; Rossi, B.; Rabourdin-Combe, C.; Gerlier, D. Human membrane cofactor protein (cd46) acts as a cellular receptor for measles virus. J. Virol. 1993, 67, 6025–6032.
Fishelson, Z.; Donin, N.; Zell, S.; Schultz, S.; Kirschfink, M. Obstacles to cancer immunotherapy: Expression of membrane complement regulatory proteins (mcrps) in tumors. Mol. Immunol. 2003, 40, 109–123, doi:10.1016/S0161-5890(03)00112-3.
[29]
Ravindranath, N.M.; Shuler, C. Expression of complement restriction factors (cd46, cd55 & cd59) in head and neck squamous cell carcinomas. J. Oral Pathol. Med. 2006, 35, 560–567, doi:10.1111/j.1600-0714.2006.00466.x.
[30]
Peng, K.W.; TenEyck, C.J.; Galanis, E.; Kalli, K.R.; Hartmann, L.C.; Russell, S.J. Intraperitoneal therapy of ovarian cancer using an engineered measles virus. Cancer Res. 2002, 62, 4656–4662.
[31]
Noyce, R.S.; Bondre, D.G.; Ha, M.N.; Lin, L.T.; Sisson, G.; Tsao, M.S.; Richardson, C.D. Tumor cell marker pvrl4 (nectin 4) is an epithelial cell receptor for measles virus. PLoS Pathog. 2011, 7, e1002240, doi:10.1371/journal.ppat.1002240.
[32]
Muhlebach, M.D.; Mateo, M.; Sinn, P.L.; Prufer, S.; Uhlig, K.M.; Leonard, V.H.; Navaratnarajah, C.K.; Frenzke, M.; Wong, X.X.; Sawatsky, B.; et al. Adherens junction protein nectin-4 is the epithelial receptor for measles virus. Nature 2011, 480, 530–533.
[33]
Racaniello, V. Virology. An exit strategy for measles virus. Science 2011, 334, 1650–1651, doi:10.1126/science.1217378.
[34]
Mendelsohn, C.L.; Wimmer, E.; Racaniello, V.R. Cellular receptor for poliovirus: Molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell 1989, 56, 855–865, doi:10.1016/0092-8674(89)90690-9.
[35]
Lopez, M.; Cocchi, F.; Menotti, L.; Avitabile, E.; Dubreuil, P.; Campadelli-Fiume, G. Nectin2alpha (prr2alpha or hveb) and nectin2delta are low-efficiency mediators for entry of herpes simplex virus mutants carrying the leu25pro substitution in glycoprotein d. J. Virol. 2000, 74, 1267–1274.
[36]
Derycke, M.S.; Pambuccian, S.E.; Gilks, C.B.; Kalloger, S.E.; Ghidouche, A.; Lopez, M.; Bliss, R.L.; Geller, M.A.; Argenta, P.A.; Harrington, K.M.; et al. Nectin 4 overexpression in ovarian cancer tissues and serum: Potential role as a serum biomarker. Am. J. Clin. Pathol. 2010, 134, 835–845, doi:10.1309/AJCPGXK0FR4MHIHB.
[37]
Takano, A.; Ishikawa, N.; Nishino, R.; Masuda, K.; Yasui, W.; Inai, K.; Nishimura, H.; Ito, H.; Nakayama, H.; Miyagi, Y.; et al. Identification of nectin-4 oncoprotein as a diagnostic and therapeutic target for lung cancer. Cancer Res. 2009, 69, 6694–6703, doi:10.1158/0008-5472.CAN-09-0016.
[38]
Fabre-Lafay, S.; Garrido-Urbani, S.; Reymond, N.; Goncalves, A.; Dubreuil, P.; Lopez, M. Nectin-4, a new serological breast cancer marker, is a substrate for tumor necrosis factor-alpha-converting enzyme (tace)/adam-17. J. Biol. Chem. 2005, 280, 19543–19550.
[39]
Sugiyama, T.; Yoneda, M.; Kuraishi, T.; Hattori, S.; Inoue, Y.; Sato, H.; Kai, C. Measles virus selectively blind to signaling lymphocyte activation molecule as a novel oncolytic virus for breast cancer treatment. Gene Ther. 2012, 20, 338–347.
[40]
Boisgerault, N.; Fonteneau, J.F.; Gregoire, M. INSERM UMR892, Nantes, France, Unpublished work. 2011.
[41]
Parrula, C.; Fernandez, S.A.; Zimmerman, B.; Lairmore, M.; Niewiesk, S. Measles virotherapy in a mouse model of adult t-cell leukaemia/lymphoma. J. Gen. Virol. 2011, 92, 1458–1466, doi:10.1099/vir.0.028910-0.
[42]
Grote, D.; Russell, S.J.; Cornu, T.I.; Cattaneo, R.; Vile, R.; Poland, G.A.; Fielding, A.K. Live attenuated measles virus induces regression of human lymphoma xenografts in immunodeficient mice. Blood 2001, 97, 3746–3754, doi:10.1182/blood.V97.12.3746.
[43]
Peng, K.W.; Ahmann, G.J.; Pham, L.; Greipp, P.R.; Cattaneo, R.; Russell, S.J. Systemic therapy of myeloma xenografts by an attenuated measles virus. Blood 2001, 98, 2002–2007, doi:10.1182/blood.V98.7.2002.
Allen, C.; Opyrchal, M.; Aderca, I.; Schroeder, M.A.; Sarkaria, J.N.; Domingo, E.; Federspiel, M.J.; Galanis, E. Oncolytic measles virus strains have significant antitumor activity against glioma stem cells. Gene Ther. 2012, 122, 745–754.
[46]
Phuong, L.K.; Allen, C.; Peng, K.W.; Giannini, C.; Greiner, S.; TenEyck, C.J.; Mishra, P.K.; Macura, S.I.; Russell, S.J.; Galanis, E.C. Use of a vaccine strain of measles virus genetically engineered to produce carcinoembryonic antigen as a novel therapeutic agent against glioblastoma multiforme. Cancer Res. 2003, 63, 2462–2469.
[47]
Iankov, I.D.; Msaouel, P.; Allen, C.; Federspiel, M.J.; Bulur, P.A.; Dietz, A.B.; Gastineau, D.; Ikeda, Y.; Ingle, J.N.; Russell, S.J.; et al. Demonstration of anti-tumor activity of oncolytic measles virus strains in a malignant pleural effusion breast cancer model. Breast Cancer Res. Treat. 2010, 122, 745–754, doi:10.1007/s10549-009-0602-z.
[48]
McDonald, C.J.; Erlichman, C.; Ingle, J.N.; Rosales, G.A.; Allen, C.; Greiner, S.M.; Harvey, M.E.; Zollman, P.J.; Russell, S.J.; Galanis, E. A measles virus vaccine strain derivative as a novel oncolytic agent against breast cancer. Breast Cancer Res. Treat. 2006, 99, 177–184.
[49]
Donnelly, O.G.; Errington-Mais, F.; Steele, L.; Hadac, E.; Jennings, V.; Scott, K.; Peach, H.; Phillips, R.M.; Bond, J.; Pandha, H.; et al. Measles virus causes immunogenic cell death in human melanoma. Gene Ther. 2011, 20, 7–15.
[50]
Meng, X.; Nakamura, T.; Okazaki, T.; Inoue, H.; Takahashi, A.; Miyamoto, S.; Sakaguchi, G.; Eto, M.; Naito, S.; Takeda, M.; et al. Enhanced antitumor effects of an engineered measles virus edmonston strain expressing the wild-type n, p, l genes on human renal cell carcinoma. Mol. Ther. 2010, 18, 544–551, doi:10.1038/mt.2009.296.
[51]
Li, H.; Peng, K.W.; Dingli, D.; Kratzke, R.A.; Russell, S.J. Oncolytic measles viruses encoding interferon beta and the thyroidal sodium iodide symporter gene for mesothelioma virotherapy. Cancer Gene Ther. 2010, 17, 550–558, doi:10.1038/cgt.2010.10.
[52]
Hutzen, B.; Pierson, C.R.; Russell, S.J.; Galanis, E.; Raffel, C.; Studebaker, A.W. Treatment of medulloblastoma using an oncolytic measles virus encoding the thyroidal sodium iodide symporter shows enhanced efficacy with radioiodine. BMC Cancer 2012, 12, 508, doi:10.1186/1471-2407-12-508.
[53]
Studebaker, A.W.; Kreofsky, C.R.; Pierson, C.R.; Russell, S.J.; Galanis, E.; Raffel, C. Treatment of medulloblastoma with a modified measles virus. Neuro. Oncol. 2010, 12, 1034–1042, doi:10.1093/neuonc/noq057.
[54]
Boisgerault, N.; Guillerme, J.B.; Pouliquen, D.; Achard, C.; Mesel-Lemoine, M.; Combredet, C.; Fonteneau, J.F.; Tangy, F.; Gregoire, M. Natural oncolytic activity of live-attenuated measles virus against human lung and colorectal adenocarcinomas. BioMed Res. Int. 2013, 2013, 387362.
[55]
Zhang, S.C.; Wang, W.L.; Cai, W.S.; Jiang, K.L.; Yuan, Z.W. Engineered measles virus edmonston strain used as a novel oncolytic viral system against human hepatoblastoma. BMC Cancer 2012, 12, 427, doi:10.1186/1471-2407-12-427.
[56]
Tangy, F.; Naim, H.Y. Live attenuated measles vaccine as a potential multivalent pediatric vaccination vector. Viral Immunol. 2005, 18, 317–326, doi:10.1089/vim.2005.18.317.
[57]
Greiner, A.; Neumann, M.; Stingl, S.; Wassink, S.; Marx, A.; Riechert, F.; Muller-Hermelink, H.K. Characterization of wue-1, a novel monoclonal antibody that stimulates the growth of plasmacytoma cell lines. Virchows. Arch. 2000, 437, 372–379, doi:10.1007/s004280000258.
[58]
Hummel, H.D.; Kuntz, G.; Russell, S.J.; Nakamura, T.; Greiner, A.; Einsele, H.; Topp, M.S. Genetically engineered attenuated measles virus specifically infects and kills primary multiple myeloma cells. J. Gen. Virol. 2009, 90, 693–701, doi:10.1099/vir.0.007302-0.
[59]
Myers, R.; Greiner, S.; Harvey, M.; Soeffker, D.; Frenzke, M.; Abraham, K.; Shaw, A.; Rozenblatt, S.; Federspiel, M.J.; Russell, S.J.; et al. Oncolytic activities of approved mumps and measles vaccines for therapy of ovarian cancer. Cancer Gene Ther. 2005, 12, 593–599, doi:10.1038/sj.cgt.7700823.
[60]
Galanis, E.; Hartmann, L.C.; Cliby, W.A.; Long, H.J.; Peethambaram, P.P.; Barrette, B.A.; Kaur, J.S.; Haluska, P.J., Jr.; Aderca, I.; Zollman, P.J.; et al. Phase i trial of intraperitoneal administration of an oncolytic measles virus strain engineered to express carcinoembryonic antigen for recurrent ovarian cancer. Cancer Res. 2010, 70, 875–882, doi:10.1158/0008-5472.CAN-09-2762.
[61]
Dingli, D.; Peng, K.W.; Harvey, M.E.; Greipp, P.R.; O’Connor, M.K.; Cattaneo, R.; Morris, J.C.; Russell, S.J. Image-guided radiovirotherapy for multiple myeloma using a recombinant measles virus expressing the thyroidal sodium iodide symporter. Blood 2004, 103, 1641–1646, doi:10.1182/blood-2003-07-2233.
[62]
Brem, H.; Gresser, I.; Grosfeld, J.; Folkman, J. The combination of antiangiogenic agents to inhibit primary tumor growth and metastasis. J. Pediatr. Surg. 1993, 28, 1253–1257, doi:10.1016/S0022-3468(05)80308-2.
[63]
Le Bon, A.; Tough, D.F. Links between innate and adaptive immunity via type i interferon. Curr. Opin. Immunol. 2002, 14, 432–436, doi:10.1016/S0952-7915(02)00354-0.
Prestwich, R.J.; Ilett, E.J.; Errington, F.; Diaz, R.M.; Steele, L.P.; Kottke, T.; Thompson, J.; Galivo, F.; Harrington, K.J.; Pandha, H.S.; et al. Immune-mediated antitumor activity of reovirus is required for therapy and is independent of direct viral oncolysis and replication. Clin. Cancer Res. 2009, 15, 4374–4381, doi:10.1158/1078-0432.CCR-09-0334.
[66]
Errington, F.; Steele, L.; Prestwich, R.; Harrington, K.J.; Pandha, H.S.; Vidal, L.; de Bono, J.; Selby, P.; Coffey, M.; Vile, R.; et al. Reovirus activates human dendritic cells to promote innate antitumor immunity. J. Immunol. 2008, 180, 6018–6026.
[67]
Kepp, O.; Tesniere, A.; Zitvogel, L.; Kroemer, G. The immunogenicity of tumor cell death. Curr. Opin. Oncol. 2009, 21, 71–76, doi:10.1097/CCO.0b013e32831bc375.
[68]
Kumar, H.; Kawai, T.; Akira, S. Pathogen recognition by the innate immune system. Int. Rev. Immunol. 2011, 30, 16–34, doi:10.3109/08830185.2010.529976.
[69]
Steinman, R.M. Decisions about dendritic cells: Past, present, and future. Annu. Rev. Immunol. 2012, 30, 1–22, doi:10.1146/annurev-immunol-100311-102839.
[70]
Steinman, R.M.; Lustig, D.S.; Cohn, Z.A. Identification of a novel cell type in peripheral lymphoid organs of mice. 3. Functional properties in vivo. J. Exp. Med. 1974, 139, 1431–1445, doi:10.1084/jem.139.6.1431.
[71]
Joffre, O.P.; Segura, E.; Savina, A.; Amigorena, S. Cross-presentation by dendritic cells. Nat. Rev. Immunol. 2012, 12, 557–569, doi:10.1038/nri3254.
[72]
Fujii, S.; Liu, K.; Smith, C.; Bonito, A.J.; Steinman, R.M. The linkage of innate to adaptive immunity via maturing dendritic cells in vivo requires cd40 ligation in addition to antigen presentation and cd80/86 costimulation. J. Exp. Med. 2004, 199, 1607–1618, doi:10.1084/jem.20040317.
[73]
Krysko, D.V.; Garg, A.D.; Kaczmarek, A.; Krysko, O.; Agostinis, P.; Vandenabeele, P. Immunogenic cell death and damps in cancer therapy. Nat. Rev. Cancer 2012, 12, 860–875, doi:10.1038/nrc3380.
[74]
Bachem, A.; Guttler, S.; Hartung, E.; Ebstein, F.; Schaefer, M.; Tannert, A.; Salama, A.; Movassaghi, K.; Opitz, C.; Mages, H.W.; et al. Superior antigen cross-presentation and xcr1 expression define human cd11c+cd141+ cells as homologues of mouse cd8+ dendritic cells. J. Exp. Med. 2010, 207, 1273–1281, doi:10.1084/jem.20100348.
[75]
Crozat, K.; Guiton, R.; Contreras, V.; Feuillet, V.; Dutertre, C.A.; Ventre, E.; Vu Manh, T.P.; Baranek, T.; Storset, A.K.; Marvel, J.; et al. The xc chemokine receptor 1 is a conserved selective marker of mammalian cells homologous to mouse cd8alpha+ dendritic cells. J. Exp. Med. 2010, 207, 1283–1292, doi:10.1084/jem.20100223.
[76]
Jongbloed, S.L.; Kassianos, A.J.; McDonald, K.J.; Clark, G.J.; Ju, X.; Angel, C.E.; Chen, C.J.; Dunbar, P.R.; Wadley, R.B.; Jeet, V.; et al. Human cd141+ (bdca-3)+ dendritic cells (dcs) represent a unique myeloid dc subset that cross-presents necrotic cell antigens. J. Exp. Med. 2010, 207, 1247–1260, doi:10.1084/jem.20092140.
[77]
Poulin, L.F.; Salio, M.; Griessinger, E.; Anjos-Afonso, F.; Craciun, L.; Chen, J.L.; Keller, A.M.; Joffre, O.; Zelenay, S.; Nye, E.; et al. Characterization of human dngr-1+ bdca3+ leukocytes as putative equivalents of mouse cd8alpha+ dendritic cells. J. Exp. Med. 2010, 207, 1261–1271, doi:10.1084/jem.20092618.
[78]
Fonteneau, J.F.; Gilliet, M.; Larsson, M.; Dasilva, I.; Munz, C.; Liu, Y.J.; Bhardwaj, N. Activation of influenza virus-specific cd4+ and cd8+ t cells: A new role for plasmacytoid dendritic cells in adaptive immunity. Blood 2003, 101, 3520–3526, doi:10.1182/blood-2002-10-3063.
[79]
Di Pucchio, T.; Chatterjee, B.; Smed-Sorensen, A.; Clayton, S.; Palazzo, A.; Montes, M.; Xue, Y.; Mellman, I.; Banchereau, J.; Connolly, J.E. Direct proteasome-independent cross-presentation of viral antigen by plasmacytoid dendritic cells on major histocompatibility complex class i. Nat. Immunol. 2008, 9, 551–557, doi:10.1038/ni.1602.
[80]
Hoeffel, G.; Ripoche, A.C.; Matheoud, D.; Nascimbeni, M.; Escriou, N.; Lebon, P.; Heshmati, F.; Guillet, J.G.; Gannage, M.; Caillat-Zucman, S.; et al. Antigen crosspresentation by human plasmacytoid dendritic cells. Immunity 2007, 27, 481–492, doi:10.1016/j.immuni.2007.07.021.
[81]
Diamond, M.S.; Kinder, M.; Matsushita, H.; Mashayekhi, M.; Dunn, G.P.; Archambault, J.M.; Lee, H.; Arthur, C.D.; White, J.M.; Kalinke, U.; et al. Type i interferon is selectively required by dendritic cells for immune rejection of tumors. J. Exp. Med. 2011, 208, 1989–2003, doi:10.1084/jem.20101158.
[82]
Fuertes, M.B.; Kacha, A.K.; Kline, J.; Woo, S.R.; Kranz, D.M.; Murphy, K.M.; Gajewski, T.F. Host type i ifn signals are required for antitumor cd8+ t cell responses through cd8{alpha}+ dendritic cells. J. Exp. Med. 2011, 208, 2005–2016, doi:10.1084/jem.20101159.
[83]
Drobits, B.; Holcmann, M.; Amberg, N.; Swiecki, M.; Grundtner, R.; Hammer, M.; Colonna, M.; Sibilia, M. Imiquimod clears tumors in mice independent of adaptive immunity by converting pdcs into tumor-killing effector cells. J. Clin. Invest. 2012, 122, 575–585, doi:10.1172/JCI61034.
[84]
Liu, C.; Lou, Y.; Lizee, G.; Qin, H.; Liu, S.; Rabinovich, B.; Kim, G.J.; Wang, Y.H.; Ye, Y.; Sikora, A.G.; et al. Plasmacytoid dendritic cells induce nk cell-dependent, tumor antigen-specific t cell cross-priming and tumor regression in mice. J. Clin. Invest. 2008, 118, 1165–1175.
[85]
Mouries, J.; Moron, G.; Schlecht, G.; Escriou, N.; Dadaglio, G.; Leclerc, C. Plasmacytoid dendritic cells efficiently cross-prime naive t cells in vivo after tlr activation. Blood 2008, 112, 3713–3722, doi:10.1182/blood-2008-03-146290.
[86]
Tel, J.; Aarntzen, E.H.; Baba, T.; Schreibelt, G.; Schulte, B.M.; Benitez-Ribas, D.; Boerman, O.C.; Croockewit, S.; Oyen, W.J.; van Rossum, M.; et al. Natural human plasmacytoid dendritic cells induce antigen-specific t-cell responses in melanoma patients. Cancer Res. 2013, 73, 1063–1075, doi:10.1158/0008-5472.CAN-12-2583.
[87]
Grote, D.; Cattaneo, R.; Fielding, A.K. Neutrophils contribute to the measles virus-induced antitumor effect: Enhancement by granulocyte macrophage colony-stimulating factor expression. Cancer Res. 2003, 63, 6463–6468.
[88]
Liu, C.; Russell, S.J.; Peng, K.W. Systemic therapy of disseminated myeloma in passively immunized mice using measles virus-infected cell carriers. Mol. Ther. 2010, 18, 1155–1164, doi:10.1038/mt.2010.43.
[89]
Mader, E.K.; Maeyama, Y.; Lin, Y.; Butler, G.W.; Russell, H.M.; Galanis, E.; Russell, S.J.; Dietz, A.B.; Peng, K.W. Mesenchymal stem cell carriers protect oncolytic measles viruses from antibody neutralization in an orthotopic ovarian cancer therapy model. Clin. Cancer Res. 2009, 15, 7246–7255, doi:10.1158/1078-0432.CCR-09-1292.
[90]
Heo, J.; Reid, T.; Ruo, L.; Breitbach, C.J.; Rose, S.; Bloomston, M.; Cho, M.; Lim, H.Y.; Chung, H.C.; Kim, C.W.; et al. Randomized dose-finding clinical trial of oncolytic immunotherapeutic vaccinia jx-594 in liver cancer. Nat. Med. 2013, 19, 329–336, doi:10.1038/nm.3089.
[91]
Taqi, A.M.; Abdurrahman, M.B.; Yakubu, A.M.; Fleming, A.F. Regression of Hodgkin’s disease after measles. Lancet 1981, 1, 1112.
[92]
Zygiert, Z. Hodgkin’s disease: Remissions after measles. Lancet 1971, 1, 593, doi:10.1016/S0140-6736(71)91186-X.
[93]
Ziegler, J.L. Spontaneous remission in burkitt’s lymphoma. Natl. Cancer Inst. Monogr. 1976, 44, 61–65.
[94]
Heinzerling, L.; Kunzi, V.; Oberholzer, P.A.; Kundig, T.; Naim, H.; Dummer, R. Oncolytic measles virus in cutaneous t-cell lymphomas mounts antitumor immune responses in vivo and targets interferon-resistant tumor cells. Blood 2005, 106, 2287–2294, doi:10.1182/blood-2004-11-4558.
[95]
ClinicalTrials.gov. Available online: http://www.clinicaltrials.gov/ (accessed on 12 December 2012).
