Adeno-associated virus activates an innate immune response in normal human cells but not in osteosarcoma cells

Journal of Virology

Volumn 85, Issue 24, 2011, Pages 13133-13143

  Laredj, Leila N ^a   Beard, Peter ^a  

^a EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; TOLL LIKE RECEPTOR 9;

ADENO ASSOCIATED VIRUS; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FIBROBLAST; HELPER VIRUS; HUMAN; HUMAN CELL; INNATE IMMUNITY; INTRACELLULAR SPACE; NONHUMAN; OSTEOSARCOMA CELL; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; SIGNAL TRANSDUCTION; VIRUS ACTIVATION; VIRUS CELL INTERACTION; VIRUS CELL TRANSFORMATION; VIRUS REPLICATION; VIRUS VIRULENCE;

CELL LINE; DEPENDOVIRUS; GENETIC VECTORS; HUMANS; IMMUNITY, INNATE; INTERFERON TYPE I; TOLL-LIKE RECEPTOR 9;

ADENO-ASSOCIATED VIRUS; DEPENDOVIRUS; PARVOVIRUS;

EID: 84855837365     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05407-11     Document Type: Article

References (51)

1. Acland, G. M., et al. 2005. Long-term restoration of rod and cone vision by single dose rAAV-mediated gene transfer to the retina in a canine model of childhood blindness. Mol. Ther. 12:1072-1082.
2. Avalos, A. M., and H. L. Ploegh. 2011. Competition by inhibitory oligonucleotides prevents binding of CpG to C-terminal TLR9. Eur. J. Immunol. 41:2820-2827.
3. Barber, G. N. Innate immune DNA sensing pathways: STING, AIMII and the regulation of interferon production and inflammatory responses. Curr. Opin. Immunol. 23:10-20.
4. Barbero, P., L. Bittova, and S. R. Pfeffer. 2002. Visualization of Rab9-mediated vesicle transport from endosomes to the trans-Golgi in living cells. J. Cell Biol. 156:511-518.
5. Bartlett, J. S., R. Wilcher, and R. J. Samulski. 2000. Infectious entry pathway of adeno-associated virus and adeno-associated virus vectors. J. Virol. 74:2777-2785.
6. Bauernfeind, F., et al. Inflammasomes: current understanding and open questions. Cell. Mol. Life Sci. 68:765-783.
7. Berns, K. I., and C. Giraud. 1996. Biology of adeno-associated virus. Curr. Top. Microbiol. Immunol. 218:1-23.
8. Bucci, C., P. Thomsen, P. Nicoziani, J. McCarthy, and B. van Deurs. 2000. Rab7: a key to lysosome biogenesis. Mol. Biol. Cell 11:467-480.
9. Chiu, Y. H., J. B. Macmillan, and Z. J. Chen. 2009. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 138:576-591.
10. Conrad, C. K., et al. 1996. Safety of single-dose administration of an adenoassociated virus (AAV)-CFTR vector in the primate lung. Gene Ther. 3:658-668.
11. Critchley-Thorne, R. J., et al. 2009. Impaired interferon signaling is a common immune defect in human cancer. Proc. Natl. Acad. Sci. U. S. A. 106:9010-9015.
12. Droemann, D., et al. 2005. Human lung cancer cells express functionally active Toll-like receptor 9. Respir. Res. 6:1.
13. Ewald, S. E., et al. Nucleic acid recognition by Toll-like receptors is coupled to stepwise processing by cathepsins and asparagine endopeptidase. J. Exp. Med. 208:643-651.
14. Geoffroy, M. C., and M. K. Chelbi-Alix. Role of promyelocytic leukemia protein in host antiviral defense. J. Interferon Cytokine Res. 31:145-158.
15. Grekova, S., et al. 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.
16. Haller, O., G. Kochs, and F. Weber. 2006. The interferon response circuit: induction and suppression by pathogenic viruses. Virology 344:119-130.
17. Hansen, J., K. Qing, and A. Srivastava. 2001. Infection of purified nuclei by adeno-associated virus 2. Mol. Ther. 4:289-296.
18. Honda, K., H. Yanai, A. Takaoka, and T. Taniguchi. 2005. Regulation of the type I IFN induction: a current view. Int. Immunol. 17:1367-1378.
19. Hornung, V., et al. 2009. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458:514-518.
20. Huang, B., J. Zhao, J. C. Unkeless, Z. H. Feng, and H. Xiong. 2008. TLR signaling by tumor and immune cells: a double-edged sword. Oncogene 27:218-224.
21. Ilvesaro, J. M., et al. 2007. Toll-like receptor-9 agonists stimulate prostate cancer invasion in vitro. Prostate 67:774-781.
22. Ingemarsdotter, C., D. Keller, and P. Beard. The DNA damage response to non-replicating adeno-associated virus: centriole overduplication and mitotic catastrophe independent of the spindle checkpoint. Virology 400:271-286.
23. Kay, M. A., et al. 2000. Evidence for gene transfer and expression of factor IX in haemophilia B patients treated with an AAV vector. Nat. Genet. 24:257-261.
24. Latz, E., et al. 2004. TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat. Immunol. 5:190-198.
25. Lee, J. W., et al. 2007. Increased Toll-like receptor 9 expression in cervical neoplasia. Mol. Carcinog. 46:941-947.
26. Martino, A. T., et al. The genome of self-complementary adeno-associated viral vectors increases Toll-like receptor 9-dependent innate immune responses in the liver. Blood 117:6459-6468.
27. Mas, A., et al. 2006. Reversal of type 1 diabetes by engineering a glucose sensor in skeletal muscle. Diabetes 55:1546-1553.
28. Matsumoto, M., and T. Seya. 2008. TLR3: interferon induction by doublestranded RNA including poly(I:C). Adv. Drug Deliv. Rev. 60:805-812.
29. Mays, L. E., and J. M. Wilson. The complex and evolving story of T cell activation to AAV vector-encoded transgene products. Mol. Ther. 19:16-27.
30. Mount, J. D., et al. 2002. Sustained phenotypic correction of hemophilia B dogs with a factor IX null mutation by liver-directed gene therapy. Blood 99:2670-2676.
31. Pajusola, K., et al. 2002. Cell-type-specific characteristics modulate the transduction efficiency of adeno-associated virus type 2 and restrain infection of endothelial cells. J. Virol. 76:11530-11540.
32. Park, B., et al. 2008. Proteolytic cleavage in an endolysosomal compartment is required for activation of Toll-like receptor 9. Nat. Immunol. 9:1407-1414.
33. Pfeffer, S. R. 2001. Rab GTPases: specifying and deciphering organelle identity and function. Trends Cell Biol. 11:487-491.
34. Qing, K., et al. 1999. Human fibroblast growth factor receptor 1 is a coreceptor for infection by adeno-associated virus 2. Nat. Med. 5:71-77.
35. Randall, R. E., and S. Goodbourn. 2008. Interferons and viruses: an interplay between induction, signaling, antiviral responses and virus countermeasures. J. Gen. Virol. 89:1-47.
36. Raykov, Z., S. Grekova, B. Leuchs, M. Aprahamian, and J. Rommelaere. 2008. Arming parvoviruses with CpG motifs to improve their oncosuppressive capacity. Int. J. Cancer 122:2880-2884.
37. Schlehofer, J. R., M. Rentrop, and D. N. Mannel. 1992. Parvoviruses are inefficient in inducing interferon-beta, tumor necrosis factor-alpha, or interleukin-6 in mammalian cells. Med. Microbiol. Immunol. 181:153-164.
38. Schmausser, B., M. Andrulis, S. Endrich, H. K. Muller-Hermelink, and M. Eck. 2005. Toll-like receptors TLR4, TLR5, and TLR9 on gastric carcinoma cells: an implication for interaction with Helicobacter pylori. Int. J. Med. Microbiol. 295:179-185.
39. 5 integrin: a coreceptor for adeno-associated virus type 2 infection. Nat. Med. 5:78-82.
40. Summerford, C., and R. J. Samulski. 1998. Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J. Virol. 72:1438-1445.
41. Takaoka, A., et al. 2007. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448:501-505.
42. Takeda, K., T. Kaisho, and S. Akira. 2003. Toll-like receptors. Annu. Rev. Immunol. 21:335-376.
43. Trischler, M., W. Stoorvogel, and O. Ullrich. 1999. Biochemical analysis of distinct Rab5- and Rab11-positive endosomes along the transferrin pathway. J. Cell Sci. 112(Pt. 24):4773-4783.
44. Unterholzner, L., et al. IFI16 is an innate immune sensor for intracellular DNA. Nat. Immunol. 11:997-1004.
45. Vandenberghe, L. H., and J. M. Wilson. 2007. AAV as an immunogen. Curr. Gene Ther. 7:325-333.
46. Wang, Z. J., K. Zhang, F. Yu. 2010. Tool-like receptors in neuroblastoma and osteosarcoma. J. Clin. Oncol. 28:e20006.
47. Xin, K. Q., et al. 2006. Induction of robust immune responses against human immunodeficiency virus is supported by the inherent tropism of adenoassociated virus type 5 for dendritic cells. J. Virol. 80:11899-11910.
48. Yakobson, B., T. Koch, and E. Winocour. 1987. Replication of adeno-associated virus in synchronized cells without the addition of a helper virus. J. Virol. 61:972-981.
49. Zaiss, A. K., et al. 2002. Differential activation of innate immune responses by adenovirus and adeno-associated virus vectors. J. Virol. 76:4580-4590.
50. Zhu, J., X. Huang, and Y. Yang. 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.
51. Zipris, D., et al. 2007. TLR9-signaling pathways are involved in Kilham rat virus-induced autoimmune diabetes in the biobreeding diabetes-resistant rat. J. Immunol. 178:693-701.