Autonomous parvoviruses neither stimulate nor are inhibited by the type I interferon response in human normal or cancer cells

Journal of Virology

Volumn 88, Issue 9, 2014, Pages 4932-4942

  Paglino, Justin C ^a   Andres, Wells ^a   van den Pol, Anthony N ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CELL PROTEIN; INTERFERON; INTERFERON STIMULATED GENE PROTEIN; OLIGOADENYLATE SYNTHETASE; PARVOVIRUS VECTOR; PROTEIN IFIT1; PROTEIN MX1; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CONTROLLED STUDY; CYTOKINE RESPONSE; CYTOMEGALOVIRUS; FIBROBLAST; GLIA CELL; GLIOMA CELL; HUMAN; HUMAN CELL; INHIBITION KINETICS; INNATE IMMUNITY; MELANOCYTE; MELANOMA CELL; NONHUMAN; PARVOVIRUS; PRIORITY JOURNAL; PROGENY; PSEUDORABIES HERPETOVIRUS; SARCOMA CELL; SIGNAL TRANSDUCTION; SINDBIS VIRUS; STRAIN DIFFERENCE; UPREGULATION; VESICULAR STOMATITIS VIRUS; VIRUS ATTENUATION; VIRUS CELL INTERACTION; VIRUS INFECTIVITY; VIRUS REPLICATION; VIRUS STRAIN;

CELL LINE; FIBROBLASTS; GENE EXPRESSION PROFILING; HUMANS; INTERFERON TYPE I; MELANOCYTES; NEUROGLIA; PARVOVIRUS;

EID: 84897529507     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03508-13     Document Type: Article

References (58)

1. Cotmore SF, Tattersall P. 2007. Parvoviral host range and cell entry mechanisms. Adv. Virus Res. 70:183-232. http://dx.doi.org/10.1016/S0065-3527(07)70005-2.
2. Farr GA, Zhang L-G, Tattersall P. 2005. Parvoviral virions deploy a capsid-tethered lipolytic enzyme to breach the endosomal membrane during cell entry. Proc. Natl. Acad. Sci. U. S. A. 102:17148-17153. http://dx.doi.org/10.1073/pnas.0508477102.
3. Suikkanen S, Aaltonen T, Nevalainen M, Välilehto O, Lindholm L, Vuento M, Vihinen-Ranta M. 2003. Exploitation of microtubule cytoskeleton and dynein during parvoviral traffic toward the nucleus. J. Virol. 77:10270-10279. http://dx.doi.org/10.1128/JVI.77.19.10270-10279.2003.
4. Ros C, Kempf C. 2004. The ubiquitin-proteasome machinery is essential for nuclear translocation of incoming minute virus of mice. Virology 324: 350-360. http://dx.doi.org/10.1016/j.virol.2004.04.016.
5. Deleu L, Pujol A, Faisst S, Rommelaere J. 1999. Activation of promoter P4 of the autonomous parvovirus minute virus of mice at early S phase is required for productive infection. J. Virol. 73:3877-3885.
6. 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.
7. Rommelaere J, Geletneky K, Angelova AL, Daeffler L, Dinsart C, Kiprianova I, Schlehofer JR, Raykov Z. 2010. Oncolytic parvoviruses as cancer therapeutics. Cytokine Growth Factor Rev. 21:185-195. http://dx.doi.org/10.1016/j.cytogfr.2010.02.011.
8. Paglino JC, Ozduman K, van den Pol AN. 2012. LuIII parvovirus selectively and efficiently targets, replicates in, and kills human glioma cells. J. Virol. 86:7280-7291. http://dx.doi.org/10.1128/JVI.00227-12.
9. Geletneky K, Kiprianova I, Ayache A, Koch R, Herrero y Calle M, Deleu L, Sommer C, Thomas N, Rommelaere J, Schlehofer JR. 2010. Regression of advanced rat and human gliomas by local or systemic treatment with oncolytic parvovirus H-1 in rat models. Neuro. Oncol. 12:804-814. http://dx.doi.org/10.1093/neuonc/noq023.
10. Grekova SP, Aprahamian M, Daeffler L, Leuchs B, Angelova A, Giese T, Galabov A, Heller A, Giese NA, Rommelaere J, Raykov Z. 2011. Interferon γ improves the vaccination potential of oncolytic parvovirus H-1PV for the treatment of peritoneal carcinomatosis in pancreatic cancer. Cancer Biol. Ther. 12:888-895. http://dx.doi.org/10.4161/cbt.12.10.17678.
11. Dempe S, Lavie M, Struyf S, Bhat R, Verbeke H, Paschek S, Berghmans N, Geibig R, Rommelaere J, Van Damme J, Dinsart C. 2012. Antitumoral activity of parvovirus-mediated IL-2 and MCP-3/CCL7 delivery into human pancreatic cancer: implication of leucocyte recruitment. Cancer Immunol. Immunother. 61:2113-2123. http://dx.doi.org/10.1007/s00262-012-1279-4.
12. Angelova AL, Aprahamian M, Balboni G, Delecluse H-J, Feederle R, Kiprianova I, Grekova SP, Galabov AS, Witzens-Harig M, Ho AD, Rommelaere J, Raykov Z. 2009. Oncolytic rat parvovirus H-1PV, a candidate for the treatment of human lymphoma: in vitro and in vivo studies. Mol. Ther. 17:1164-1172. http://dx.doi.org/10.1038/mt.2009.78.
13. Dupont F. 2003. Risk assessment of the use of autonomous parvovirusbased vectors. Curr. Gene Ther. 3:567-582. http://dx.doi.org/10.2174/1566523034578104.
14. Nüesch JPF, Lacroix J, Marchini A, Rommelaere J. 2012. Molecular pathways: rodent parvoviruses-mechanisms of oncolysis and prospects for clinical cancer treatment. Clin. Cancer Res. 18:3516-3523. http://dx.doi.org/10.1158/1078-0432.CCR-11-2325.
15. Fuks F, Deleu L, Dinsart C, Rommelaere J, Faisst S. 1996. ras oncogenedependent activation of the P4 promoter of minute virus of mice through a proximal P4 element interacting with the Ets family of transcription factors. J. Virol. 70:1331-1339.
16. Perros M, Deleu L, Vanacker JM, Kherrouche Z, Spruyt N, Faisst S, Rommelaere J. 1995. Upstream CREs participate in the basal activity of minute virus of mice promoter P4 and in its stimulation in rastransformed cells. J. Virol. 69:5506-5515.
17. Wollmann G, Ozduman K, van den Pol AN. 2012. Oncolytic virus therapy for glioblastoma multiforme: concepts and candidates. Cancer J. 18:69-81. http://dx.doi.org/10.1097/PPO.0b013e31824671c9.
18. 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.
19. Chen H-M, Tanaka N, Mitani Y, Oda E, Nozawa H, Chen J-Z, Yanai H, Negishi H, Choi MK, Iwasaki T, Yamamoto H, Taniguchi T, Takaoka A. 2009. Critical role for constitutive type I interferon signaling in the prevention of cellular transformation. Cancer Sci. 100:449-456. http://dx.doi.org/10.1111/j.1349-7006.2008.01051.x.
20. Katsoulidis E, Kaur S, Platanias LC. 2010. Deregulation of interferon signaling in malignant cells. Pharmaceuticals 3:406-418. http://dx.doi.org/10.3390/ph3020406.
21. Grekova S, Zawatzky R, Hörlein R, Cziepluch C, Mincberg M, Davis C, Rommelaere J, Daeffler L. 2010. Activation of an antiviral response in normal but not transformed mouse cells: a new determinant of minute virus of mice oncotropism. J. Virol. 84:516-531. http://dx.doi.org/10.1128/JVI.01618-09.
22. Mattei LM, Cotmore SF, Tattersall P, Iwasaki A. 2013. Parvovirus evades interferon-dependent viral control in primary mouse embryonic fibroblasts. Virology 442:20-27. http://dx.doi.org/10.1016/j.virol.2013.03.020.
23. Raykov Z, Grekova SP, Hörlein R, Leuchs B, Giese T, Giese NA, Rommelaere J, Zawatzky R, Daeffler L. 2013. TLR-9 contributes to the antiviral innate immune sensing of rodent parvoviruses MVMp and H-1PV by normal human immune cells. PLoS One 8:e55086. http://dx.doi.org/10.1371/journal.pone.0055086.
24. Barber GN. 2004. Vesicular stomatitis virus as an oncolytic vector. Viral Immunol. 17:516-527. http://dx.doi.org/10.1089/vim.2004.17.516.
25. Stojdl DF, Lichty B, Knowles S, Marius R, Atkins H, Sonenberg N, Bell JC. 2000. Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat. Med. 6:821-825. http://dx.doi.org/10.1038/77558.
26. Hastie E, Grdzelishvili VZ. 2012. Vesicular stomatitis virus as a flexible platform for oncolytic virotherapy against cancer. J. Gen. Virol. 93(Pt 12):2529-2545. http://dx.doi.org/10.1099/vir.0.046672-0.
27. Wollmann G, Rogulin V, Simon I, Rose JK, van den Pol AN. 2010. Some attenuated variants of vesicular stomatitis virus show enhanced oncolytic activity against human glioblastoma cells relative to normal brain cells. J. Virol. 84:1563-1573. http://dx.doi.org/10.1128/JVI.02040-09.
28. Paglino JC, van den Pol AN. 2011. Vesicular stomatitis virus has extensive oncolytic activity against human sarcomas: rare resistance is overcome by blocking interferon pathways. J. Virol. 85:9346-9358. http://dx.doi.org/10.1128/JVI.00723-11.
29. Wollmann G, Davis JN, Bosenberg MW, van den Pol AN. 2013. Vesicular stomatitis virus variants selectively infect and kill human melanomas but not normal melanocytes. J. Virol. 87:6644-6659. http://dx.doi.org/10.1128/JVI.03311-12.
30. Tworkoski K, Singhal G, Szpakowski S, Zito CI, Bacchiocchi A, Muthusamy V, Bosenberg M, Krauthammer M, Halaban R, Stern DF. 2011. Phosphoproteomic screen identifies potential therapeutic targets in melanoma. Mol. Cancer Res. 9:801-812. http://dx.doi.org/10.1158/1541-7786.MCR-10-0512.
31. Tattersall P, Bratton J. 1983. Reciprocal productive and restrictive viruscell interactions of immunosuppressive and prototype strains of minute virus of mice. J. Virol. 46:944-955.
32. Wollmann G, Tattersall P, van den Pol AN. 2005. Targeting human glioblastoma cells: comparison of nine viruses with oncolytic potential. J. Virol. 79:6005-6022. http://dx.doi.org/10.1128/JVI.79.10.6005-6022.2005.
33. Paglino J, Tattersall P. 2011. The parvoviral capsid controls an intracellular phase of infection essential for efficient killing of stepwisetransformed human fibroblasts. Virology 416:32-41. http://dx.doi.org/10.1016/j.virol.2011.04.015.
34. Gray SJ, Foti SB, Schwartz JW, Bachaboina L, Taylor-Blake B, Coleman J, Ehlers MD, Zylka MJ, McCown TJ, Samulski RJ. 2011. Optimizing promoters for recombinant adeno-associated virus-mediated gene expression in the peripheral and central nervous system using selfcomplementary vectors. Hum. Gene Ther. 22:1143-1153. http://dx.doi.org/10.1089/hum.2010.245.
35. Ball-Goodrich LJ, Tattersall P. 1992. Two amino acid substitutions within the capsid are coordinately required for acquisition of fibrotropism by the lymphotropic strain of minute virus of mice. J. Virol. 66:3415-3423.
36. Haller O, Kochs G, Weber F. 2007. Interferon, Mx, and viral countermeasures. Cytokine Growth Factor Rev. 18:425-433. http://dx.doi.org/10.1016/j.cytogfr.2007.06.001.
37. Der SD, Zhou A, Williams BR, Silverman RH. 1998. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc. Natl. Acad. Sci. U. S. A. 95:15623-15628. http://dx.doi.org/10.1073/pnas.95.26.15623.
38. Rieder M, Conzelmann K-K. 2009. Rhabdovirus evasion of the interferon system. J. Interferon Cytokine Res. 29:499-509. http://dx.doi.org/10.1089/jir.2009.0068.
39. Newton K, Dixit VM. 2012. Signaling in innate immunity and inflammation. Cold Spring Harb. Perspect. Biol. 4:a006049. http://dx.doi.org/10.1101/cshperspect.a006049.
40. Barber GN. 2005. VSV-tumor selective replication and protein translation. Oncogene 24:7710-7719. http://dx.doi.org/10.1038/sj.onc.1209042.
41. Biswas M, Kumar SRP, Allen A, Yong W, Nimmanapalli R, Samal SK, Elankumaran S. 2012. Cell-type-specific innate immune response to oncolytic Newcastle disease virus. Viral Immunol. 25:268-276. http://dx.doi.org/10.1089/vim.2012.0020.
42. Wollmann G, Robek MD, van den Pol AN. 2007. Variable deficiencies in the interferon response enhance susceptibility to vesicular stomatitis virus oncolytic actions in glioblastoma cells but not in normal human glial cells. J. Virol. 81:1479-1491. http://dx.doi.org/10.1128/JVI.01861-06.
43. Nam H-J, Gurda-Whitaker B, Gan WY, Ilaria S, McKenna R, Mehta P, Alvarez RA, Agbandje-McKenna M. 2006. Identification of the sialic acid structures recognized by minute virus of mice and the role of binding affinity in virulence adaptation. J. Biol. Chem. 281:25670-25677. http://dx.doi.org/10.1074/jbc.M604421200.
44. Spalholz BA, Tattersall P. 1983. Interaction of minute virus of mice with differentiated cells: strain-dependent target cell specificity is mediated by intracellular factors. J. Virol. 46:937-943.
45. Lang SI, Boelz S, Stroh-Dege AY, Rommelaere J, Dinsart C, Cornelis JJ. 2005. The infectivity and lytic activity of minute virus of mice wild-type and derived vector particles are strikingly different. J. Virol. 79:289-298. http://dx.doi.org/10.1128/JVI.79.1.289-298.2005.
46. Mattei LM, Cotmore SF, Li L, Tattersall P, Iwasaki A. 2013. Toll-like receptor 9 in plasmacytoid dendritic cells fails to detect parvoviruses. J. Virol. 87:3605-3608. http://dx.doi.org/10.1128/JVI.03155-12.
47. Hornung V, Latz E. 2010. Intracellular DNA recognition. Nat. Rev. Immunol. 10:123-130. http://dx.doi.org/10.1038/nri2690.
48. Hornung V, Rothenfusser S, Britsch S, Krug A, Jahrsdörfer B, Giese T, Endres S, Hartmann G. 2002. Quantitative expression of Toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J. Immunol. 168: 4531-4537.
49. Hanten JA, Vasilakos JP, Riter CL, Neys L, Lipson KE, Alkan SS, Birmachu W. 2008. Comparison of human B cell activation by TLR7 and TLR9 agonists. BMC Immunol. 9:39. http://dx.doi.org/10.1186/1471-2172-9-39.
50. Mani B, Baltzer C, Valle N, Almendral JM, Kempf C, Ros C. 2006. Low pH-dependent endosomal processing of the incoming parvovirus minute virus of mice virion leads to externalization of the VP1 N-terminal sequence (N-VP1), N-VP2 cleavage, and uncoating of the full-length genome. J. Virol. 80:1015-1024. http://dx.doi.org/10.1128/JVI.80.2.1015-1024.2006.
51. Paludan SR, Bowie AG. 2013. Immune sensing of DNA. Immunity 38: 870-880. http://dx.doi.org/10.1016/j.immuni.2013.05.004.
52. Burdette DL, Vance RE. 2013. STING and the innate immune response to nucleic acids in the cytosol. Nat. Immunol. 14:19-26. http://dx.doi.org/10.1038/ni.2491.
53. Ventoso I, Berlanga JJ, Almendral JM. 2010. Translation control by protein kinase R restricts minute virus of mice infection: role in parvovirus oncolysis. J. Virol. 84:5043-5051. http://dx.doi.org/10.1128/JVI.02188-09.
54. Goubau D, Deddouche S, Reis e Sousa C. 2013. Cytosolic sensing of viruses. Immunity 38:855-869. http://dx.doi.org/10.1016/j.immuni.2013.05.007.
55. Rogers GL, Martino AT, Aslanidi GV, Jayandharan GR, Srivastava A, Herzog RW. 2011. Innate immune responses to AAV vectors. Front. Microbiol. 2:194. http://dx.doi.org/10.3389/fmicb.2011.00194.
56. Zhu J, Huang X, Yang Y. 2009. The TLR9-MyD88 pathway is critical for adaptive immune responses to adeno-associated virus gene therapy vectors in mice. J. Clin. Invest. 119:2388-2398. http://dx.doi.org/10.1172/JCI37607.
57. Laredj LN, Beard P. 2011. Adeno-associated virus activates an innate immune response in normal human cells but not in osteosarcoma cells. J. Virol. 85:13133-13143. http://dx.doi.org/10.1128/JVI.05407-11.
58. Jayandharan GR, Aslanidi G, Martino AT, Jahn SC, Perrin GQ, Herzog RW, Srivastava A. 2011. Activation of the NF-kappaB pathway by adenoassociated virus (AAV) vectors and its implications in immune response and gene therapy. Proc. Natl. Acad. Sci. U. S. A. 108:3743-3748. http://dx.doi.org/10.1073/pnas.1012753108.