Blockade of type I interferon (IFN) production by retroviral replicating vectors and reduced tumor cell responses to IFN likely contribute to tumor selectivity

Journal of Virology

Volumn 88, Issue 17, 2014, Pages 10066-10077

  Lin, Amy H ^a   Burrascano, Cindy ^a   Pettersson, Par L ^a   Ibañez, Carlos E ^a   Gruber, Harry E ^a   Jolly, Douglas J ^a  

^a Tocagen Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON;

CELL CULTURE; GENETICS; HUMAN; IMMUNOLOGY; MOLONEY MURINE LEUKEMIA VIRUS; NEOPLASM; PHYSIOLOGY; SECRETION (PROCESS); VIRUS REPLICATION;

CELLS, CULTURED; HUMANS; INTERFERON TYPE I; MOLONEY MURINE LEUKEMIA VIRUS; NEOPLASMS; VIRUS REPLICATION;

EID: 84921955318     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02300-13     Document Type: Article

References (44)

1. Prestwich RJ, Errington F, Diaz RM, Pandha HS, Harrington KJ, Melcher AA, Vile RG. 2009. The case of oncolytic viruses versus the immune system: waiting on the judgment of Solomon. Hum. Gene Ther. 20:1119-1132. http://dx.doi.org/10.1089/hum.2009.135.
2. Ostertag D, Amundson KK, Lopez Espinoza F, Martin B, Buckley T, Galvao da Silva AP, Lin AH, Valenta DT, Perez OD, Ibanez CE, Chen CI, Pettersson PL, Burnett R, Daublebsky V, Hlavaty J, Gunzburg W, Kasahara N, Gruber HE, Jolly DJ, Robbins JM. 2012. Brain tumor eradication and prolonged survival from intratumoral conversion of 5-fluorocytosine to 5-fluorouracil using a nonlytic retroviral replicating vector. Neuro Oncol. 14:145-159. http://dx.doi.org/10.1093/neuonc/nor199.
3. Wang W, Tai CK, Kershaw AD, Solly SK, Klatzmann D, Kasahara N, Chen TC. 2006. Use of replication-competent retroviral vectors in an immunocompetent intracranial glioma model. Neurosurg. Focus 20:E25. http://dx.doi.org/10.3171/foc.2006.20.4.1.
4. Cornetta K, Moen RC, Culver K, Morgan RA, McLachlin JR, Sturm S, Selegue J, London W, Blaese RM, Anderson WF. 1990. Amphotropic murine leukemia retrovirus is not an acute pathogen for primates. Hum. Gene Ther. 1:15-30. http://dx.doi.org/10.1089/hum.1990.1.1-15.
5. Perez OD, Logg CR, Hiraoka K, Diago O, Burnett R, Inagaki A, Jolson D, Amundson K, Buckley T, Lohse D, Lin A, Burrascano C, Ibanez C, Kasahara N, Gruber HE, Jolly DJ. 2012. Design and selection of Toca 511 for clinical use: modified retroviral replicating vector with improved stability and gene expression. Mol. Ther. 20:1689-1698. http://dx.doi.org/10.1038/mt.2012.83.
6. Yamashita M, Emerman M. 2006. Retroviral infection of non-dividing cells: old and new perspectives. Virology 344:88-93. http://dx.doi.org/10.1016/j.virol.2005.09.012.
7. Stojdl DF, Lichty BD, ten Oever BR, Paterson JM, Power AT, Knowles S, Marius R, Reynard J, Poliquin L, Atkins H, Brown EG, Durbin RK, Durbin JE, Hiscott J, Bell JC. 2003. VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer Cell 4:263-275. http://dx.doi.org/10.1016/S1535-6108(03)00241-1.
8. Janeway CA, Jr, Medzhitov R. 2002. Innate immune recognition. Annu. Rev. Immunol. 20:197-216. http://dx.doi.org/10.1146/annurev.immunol.20.083001.084359.
9. Wolf D, Goff SP. 2008. Host restriction factors blocking retroviral replication. Annu. Rev. Genet. 42:143-163. http://dx.doi.org/10.1146/annurev.genet.42.110807.091704.
10. Nakhaei P, Hiscott J, Lin R. 2010. STING-ing the antiviral pathway. J. Mol. Cell Biol. 2:110-112. http://dx.doi.org/10.1093/jmcb/mjp048.
11. Randall RE, Goodbourn S. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 89:1-47. http://dx.doi.org/10.1099/vir.0.83391-0.
12. Cerami E, Demir E, Schultz N, Taylor BS, Sander C. 2010. Automated network analysis identifies core pathways in glioblastoma. PLoS One 5:e8918. http://dx.doi.org/10.1371/journal.pone.0008918.
13. Marozin S, Altomonte J, Stadler F, Thasler WE, Schmid RM, Ebert O. 2008. Inhibition of the IFN-beta response in hepatocellular carcinoma by alternative spliced isoform of IFN regulatory factor-3. Mol. Ther. 16: 1789-1797. http://dx.doi.org/10.1038/mt.2008.201.
14. Wong LH, Krauer KG, Hatzinisiriou I, Estcourt MJ, Hersey P, Tam ND, Edmondson S, Devenish RJ, Ralph SJ. 1997. Interferon-resistant human melanoma cells are deficient in ISGF3 components, STAT1, STAT2, and p48-ISGF3+. J. Biol. Chem. 272:28779-28785. http://dx.doi.org/10.1074/jbc.272.45.28779.
15. Burns JC, Friedmann T, Driever W, Burrascano M, Yee JK. 1993. Vesicular stomatitis virus G glycoprotein pseudotyped retroviral vectors: concentration to very high titer and efficient gene transfer into mammalian and nonmammalian cells. Proc. Natl. Acad. Sci. U. S. A. 90:8033-8037. http://dx.doi.org/10.1073/pnas.90.17.8033.
16. Sheridan PL, Bodner M, Lynn A, Phuong TK, DePolo NJ, de la Vega DJ, Jr, O'Dea J, Nguyen K, McCormack JE, Driver DA, Townsend K, Ibanez CE, Sajjadi NC, Greengard JS, Moore MD, Respess J, Chang SM, Dubensky TW, Jr, Jolly DJ, Sauter SL. 2000. Generation of retroviral packaging and producer cell lines for large-scale vector production and clinical application: improved safety and high titer. Mol. Ther. 2:262-275. http://dx.doi.org/10.1006/mthe.2000.0123.
17. Andreadis ST, Brott D, Fuller AO, Palsson BO. 1997. Moloney murine leukemia virus-derived retroviral vectors decay intracellularly with a halflife in the range of 5.5 to 7.5 hours. J. Virol. 71:7541-7548.
18. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, Trono D, Naldini L. 1998. A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72:8463-8471.
19. Rulli SJ, Jr, Mirro J, Hill SA, Lloyd P, Gorelick RJ, Coffin JM, Derse D, Rein A. 2008. Interactions of murine APOBEC3 and human APOBEC3G with murine leukemia viruses. J. Virol. 82:6566-6575. http://dx.doi.org/10.1128/JVI.01357-07.
20. Santiago ML, Montano M, Benitez R, Messer RJ, Yonemoto W, Chesebro B, Hasenkrug KJ, Greene WC. 2008. Apobec3 encodes Rfv3, a gene influencing neutralizing antibody control of retrovirus infection. Science 321:1343-1346. http://dx.doi.org/10.1126/science.1161121.
21. Noser JA, Mael AA, Sakuma R, Ohmine S, Marcato P, Lee PW, Ikeda Y. 2007. The RAS/Raf1/MEK/ERK signaling pathway facilitates VSVmediated oncolysis: implication for the defective interferon response in cancer cells. Mol. Ther. 15:1531-1536. http://dx.doi.org/10.1038/sj.mt.6300193.
22. da Silva AJ, Brickelmaier M, Majeau GR, Lukashin AV, Peyman J, Whitty A, Hochman PS. 2002. Comparison of gene expression patterns induced by treatment of human umbilical vein endothelial cells with IFN-alpha 2b vs. IFN-beta 1a: understanding the functional relationship between distinct type I interferons that act through a common receptor. J. Interferon Cytokine Res. 22:173-188. http://dx.doi.org/10.1089/107999002753536149.
23. Pomykala HM, Bohlander SK, Broeker PL, Olopade OI, Diaz MO. 1994. Breakpoint junctions of chromosome 9p deletions in two human glioma cell lines. Mol. Cell. Biol. 14:7604-7610.
24. Raj NB, Pitha PM. 1981. Analysis of interferon mRNA in human fibroblast cells induced to produce interferon. Proc. Natl. Acad. Sci. U. S. A. 78:7426-7430. http://dx.doi.org/10.1073/pnas.78.12.7426.
25. Kadowaki N, Ho S, Antonenko S, Malefyt RW, Kastelein RA, Bazan F, Liu YJ. 2001. Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J. Exp. Med. 194:863-869. http://dx.doi.org/10.1084/jem.194.6.863.
26. Brown BD, Sitia G, Annoni A, Hauben E, Sergi LS, Zingale A, Roncarolo MG, Guidotti LG, Naldini L. 2007. In vivo administration of lentiviral vectors triggers a type I interferon response that restricts hepatocyte gene transfer and promotes vector clearance. Blood 109:2797-2805. http://dx.doi.org/10.1182/blood-2006-10-049312.
27. Abe A, Chen ST, Miyanohara A, Friedmann T. 1998. In vitro cell-free conversion of noninfectious Moloney retrovirus particles to an infectious form by the addition of the vesicular stomatitis virus surrogate envelopeG protein. J. Virol. 72:6356-6361.
28. Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa C. 2004. Innate antiviral responses by means of TLR7-mediated recognition of singlestranded RNA. Science 303:1529-1531. http://dx.doi.org/10.1126/science.1093616.
29. Edwards SA, Fan H. 1979. gag-Related polyproteins of Moloney murine leukemia virus: evidence for independent synthesis of glycosylated and unglycosylated forms. J. Virol. 30:551-563.
30. Fujisawa R, McAtee FJ, Favara C, Hayes SF, Portis JL. 2001. N-terminal cleavage fragment of glycosylated Gag is incorporated into murine oncornavirus particles. J. Virol. 75:11239-11243. http://dx.doi.org/10.1128/JVI.75.22.11239-11243.2001.
31. Stavrou S, Nitta T, Kotla S, Ha D, Nagashima K, Rein AR, Fan H, Ross SR. 2013. Murine leukemia virus glycosylated Gag blocks apolipoprotein B editing complex 3 and cytosolic sensor access to the reverse transcription complex. Proc. Natl. Acad. Sci. U. S. A. 110:9078-9083. http://dx.doi.org/10.1073/pnas.1217399110.
32. Mangeney M, Heidmann T. 1998. Tumor cells expressing a retroviral envelope escape immune rejection in vivo. Proc. Natl. Acad. Sci. U. S. A. 95:14920-14925. http://dx.doi.org/10.1073/pnas.95.25.14920.
33. Schmidt DM, Sidhu NK, Cianciolo GJ, Snyderman R. 1987. Recombinant hydrophilic region of murine retroviral protein p15E inhibits stimulated T-lymphocyte proliferation. Proc. Natl. Acad. Sci. U. S. A. 84:7290-7294. http://dx.doi.org/10.1073/pnas.84.20.7290.
34. Gerlach N, Schimmer S, Weiss S, Kalinke U, Dittmer U. 2006. Effects of type I interferons on Friend retrovirus infection. J. Virol. 80:3438-3444. http://dx.doi.org/10.1128/JVI.80.7.3438-3444.2006.
35. Browne EP. 2011. Toll-like receptor 7 controls the anti-retroviral germinal center response. PLoS Pathog. 7:e1002293. http://dx.doi.org/10.1371/journal.ppat.1002293.
36. Kane M, Case LK, Wang C, Yurkovetskiy L, Dikiy S, Golovkina TV. 2011. Innate immune sensing of retroviral infection via Toll-like receptor 7 occurs upon viral entry. Immunity 35:135-145. http://dx.doi.org/10.1016/j.immuni.2011.05.011.
37. Schlender J, Hornung V, Finke S, Gunthner-Biller M, Marozin S, Brzozka K, Moghim S, Endres S, Hartmann G, Conzelmann KK. 2005. Inhibition of toll-like receptor 7-and 9-mediated alpha/beta interferon production in human plasmacytoid dendritic cells by respiratory syncytial virus and measles virus. J. Virol. 79:5507-5515. http://dx.doi.org/10.1128/JVI.79.9.5507-5515.2005.
38. Santos S, Obukhov Y, Nekhai S, Bukrinsky M, Iordanskiy S. 2012. Virus-producing cells determine the host protein profiles of HIV-1 virion cores. Retrovirology 9:65. http://dx.doi.org/10.1186/1742-4690-9-65.
39. Gao D, Wu J, Wu YT, Du F, Aroh C, Yan N, Sun L, Chen ZJ. 2013. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341:903-906. http://dx.doi.org/10.1126/science.1240933.
40. Kim T, Pazhoor S, Bao M, Zhang Z, Hanabuchi S, Facchinetti V, Bover L, Plumas J, Chaperot L, Qin J, Liu YJ. 2010. Aspartate-glutamatealanine-histidine box motif (DEAH)/RNA helicase A helicases sense microbial DNA in human plasmacytoid dendritic cells. Proc. Natl. Acad. Sci. U. S. A. 107:15181-15186. http://dx.doi.org/10.1073/pnas.1006539107.
41. Yan N, Regalado-Magdos AD, Stiggelbout B, Lee-Kirsch MA, Lieberman J. 2010. The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat. Immunol. 11:1005-1013. http://dx.doi.org/10.1038/ni.1941.
42. Yanai H, Ban T, Wang Z, Choi MK, Kawamura T, Negishi H, Nakasato M, Lu Y, Hangai S, Koshiba R, Savitsky D, Ronfani L, Akira S, Bianchi ME, Honda K, Tamura T, Kodama T, Taniguchi T. 2009. HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature 462:99-103. http://dx.doi.org/10.1038/nature08512.
43. Agudo J, Ruzo A, Kitur K, Sachidanandam R, Blander JM, Brown BD. 2012. A TLR and non-TLR mediated innate response to lentiviruses restricts hepatocyte entry and can be ameliorated by pharmacological blockade. Mol. Ther. 20:2257-2267. http://dx.doi.org/10.1038/mt.2012.150.
44. Shanker A, Marincola FM. 2011. Cooperativity of adaptive and innate immunity: implications for cancer therapy. Cancer Immunol. Immunother. 60:1061-1074. http://dx.doi.org/10.1007/s00262-011-1053-z.