1887

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Volume 88, Issue 4

Adenovirus vector delivery stimulates natural killer cell recognition Free

Abstract

We report that delivery of first-generation replication-deficient adenovirus (RDAd) vectors into primary human fibroblasts is associated with the induction of natural killer (NK) cell-mediated cytolysis . RDAd vector delivery induced cytolysis by a range of NK cell populations including the NK cell clone NKL, primary polyclonal NK lines and a proportion of NK clones (36 %) in autologous HLA-matched assays. Adenovirus-induced cytolysis was inhibited by antibody blocking of the NK-activating receptor NKG2D, implicating this receptor in this function. NKG2D is ubiquitously expressed on NK cells and CD8 T cells. Significantly, -irradiation of the vector eliminated the effect, suggesting that breakthrough expression from the vector induces at least some of the pro-inflammatory responses of unknown aetiology following the application of RDAd vectors during gene delivery.

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2007-04-01
2024-04-26
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References

  1. Aldemir H., Prod'homme V., Dumaurier M. J., Retiere C., Poupon G., Cazareth J., Bihl F., Braud V. M. 2005; Cutting edge: lectin-like transcript 1 is a ligand for the CD161 receptor. J Immunol 175:7791–7795 [CrossRef]
     [Google Scholar]
  2. Bacon L., Eagle R. A., Meyer M., Easom N., Young N. T., Trowsdale J. 2004; Two human ULBP/RAET1 molecules with transmembrane regions are ligands for NKG2D. J Immunol 173:1078–1084 [CrossRef]
     [Google Scholar]
  3. Bauer S., Groh V., Wu J., Steinle A., Phillips J. H., Lanier L. L., Spies T. 1999; Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285:727–729 [CrossRef]
     [Google Scholar]
  4. Borgland S. L., Bowen G. P., Wong N. C., Libermann T. A., Muruve D. A. 2000; Adenovirus vector-induced expression of the C–X-C chemokine IP-10 is mediated through capsid-dependent activation of NF-kappaB. J Virol 74:3941–3947 [CrossRef]
     [Google Scholar]
  5. Bottino C., Castriconi R., Pende D., Rivera P., Nanni M., Carnemolla B., Cantoni C., Grassi J., Marcenaro S. other authors 2003; Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. J Exp Med 198:557–567 [CrossRef]
     [Google Scholar]
  6. Chalupny N. J., Sutherland C. L., Lawrence W. A., Rein-Weston A., Cosman D. 2003; ULBP4 is a novel ligand for human NKG2D. Biochem Biophys Res Commun 305:129–135 [CrossRef]
     [Google Scholar]
  7. Cosman D., Fanger N., Borges L., Kubin M., Chin W., Peterson L., Hsu M. L. 1997; A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 7:273–282 [CrossRef]
     [Google Scholar]
  8. Cosman D., Mullberg J., Sutherland C. L., Chin W., Armitage R., Fanslow W., Kubin M., Chalupny N. J. 2001; ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 14:123–133 [CrossRef]
     [Google Scholar]
  9. Crystal R. G., McElvaney N. G., Rosenfeld M. A., Chu C. S., Mastrangeli A., Hay J. G., Brody S. L., Jaffe H. A., Eissa N. T., Danel C. 1994; Administration of an adenovirus containing the human CFTR cDNA to the respiratory tract of individuals with cystic fibrosis. Nat Genet 8:42–51 [CrossRef]
     [Google Scholar]
  10. Dunn C., Chalupny N. J., Sutherland C. L., Dosch S., Sivakumar P. V., Johnson D. C., Cosman D. 2003; Human cytomegalovirus glycoprotein UL16 causes intracellular sequestration of NKG2D ligands, protecting against natural killer cell cytotoxicity. J Exp Med 197:1427–1439 [CrossRef]
     [Google Scholar]
  11. Fooks A. R., Schadeck E., Liebert U. G., Dowsett A. B., Rima B. K., Steward M., Stephenson J. R., Wilkinson G. W. 1995; High-level expression of the measles virus nucleocapsid protein by using a replication-deficient adenovirus vector: induction of an MHC-1-restricted CTL response and protection in a murine model. Virology 210:456–465 [CrossRef]
     [Google Scholar]
  12. Friese M. A., Platten M., Lutz S. Z., Naumann U., Aulwurm S., Bischof F., Buhring H. J., Dichgans J., Rammensee H. G. other authors 2003; MICA/NKG2D-mediated immunogene therapy of experimental gliomas. Cancer Res 63:8996–9006
     [Google Scholar]
  13. Fuchs A., Cella M., Giurisato E., Shaw A. S., Colonna M. 2004; Cutting edge: CD96 (tactile) promotes NK cell-target cell adhesion by interacting with the poliovirus receptor (CD155). J Immunol 172:3994–3998 [CrossRef]
     [Google Scholar]
  14. Gasser S., Orsulic S., Brown E. J., Raulet D. H. 2005; The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 436:1186–1190 [CrossRef]
     [Google Scholar]
  15. Griffin C., Wang E. C., McSharry B. P., Rickards C., Browne H., Wilkinson G. W., Tomasec P. 2005; Characterization of a highly glycosylated form of the human cytomegalovirus HLA class I homologue gpUL18. J Gen Virol 86:2999–3008 [CrossRef]
     [Google Scholar]
  16. Groh V., Bahram S., Bauer S., Herman A., Beauchamp M., Spies T. 1996; Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc Natl Acad Sci U S A 93:12445–12450 [CrossRef]
     [Google Scholar]
  17. Groh V., Steinle A., Bauer S., Spies T. 1998; Recognition of stress-induced MHC molecules by intestinal epithelial gammadelta T cells. Science 279:1737–1740 [CrossRef]
     [Google Scholar]
  18. Groh V., Rhinehart R., Randolph-Habecker J., Topp M. S., Riddell S. R., Spies T. 2001; Costimulation of CD8alphabeta T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat Immunol 2:255–260 [CrossRef]
     [Google Scholar]
  19. He T. C., Zhou S., da Costa L. T., Yu J., Kinzler K. W., Vogelstein B. 1998; A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci U S A 95:2509–2514 [CrossRef]
     [Google Scholar]
  20. Lanier L. L. 2005; NK cell recognition. Annu Rev Immunol 23:225–274 [CrossRef]
     [Google Scholar]
  21. Li E., Stupack D., Klemke R., Cheresh D. A., Nemerow G. R. 1998; Adenovirus endocytosis via alpha(v) integrins requires phosphoinositide-3-OH kinase. J Virol 72:2055–2061
     [Google Scholar]
  22. Liu Q., Muruve D. A. 2003; Molecular basis of the inflammatory response to adenovirus vectors. Gene Ther 10:935–940 [CrossRef]
     [Google Scholar]
  23. Marshall E. 1999; Gene therapy death prompts review of adenovirus vector. Science 286:2244–2245 [CrossRef]
     [Google Scholar]
  24. McGrory W. J., Bautista D. S., Graham F. L. 1988; A simple technique for the rescue of early region I mutations into infectious human adenovirus type 5. Virology 163:614–617 [CrossRef]
     [Google Scholar]
  25. McSharry B. P., Jones C. J., Skinner J. W., Kipling D., Wilkinson G. W. 2001; Human telomerase reverse transcriptase-immortalized MRC-5 and HCA2 human fibroblasts are fully permissive for human cytomegalovirus. J Gen Virol 82:855–863
     [Google Scholar]
  26. Morris R. J., Chong L. K., Wilkinson G. W., Wang E. C. 2005; A high-efficiency system of natural killer cell cloning. J Immunol Methods 307:24–33 [CrossRef]
     [Google Scholar]
  27. Muruve D. A. 2004; The innate immune response to adenovirus vectors. Hum Gene Ther 15:1157–1166 [CrossRef]
     [Google Scholar]
  28. Muruve D. A., Cotter M. J., Zaiss A. K., White L. R., Liu Q., Chan T., Clark S. A., Ross P. J., Meulenbroek R. A. other authors 2004; Helper-dependent adenovirus vectors elicit intact innate but attenuated adaptive host immune responses in vivo. J Virol 78:5966–5972 [CrossRef]
     [Google Scholar]
  29. Nakajima H., Cella M., Langen H., Friedlein A., Colonna M. 1999; Activating interactions in human NK cell recognition: the role of 2B4–CD48. Eur J Immunol 29:1676–1683 [CrossRef]
     [Google Scholar]
  30. Philpott N. J., Nociari M., Elkon K. B., Falck-Pedersen E. 2004; Adenovirus-induced maturation of dendritic cells through a PI3 kinase-mediated TNF-alpha induction pathway. Proc Natl Acad Sci U S A 101:6200–6205 [CrossRef]
     [Google Scholar]
  31. Rafii S., Dias S., Meeus S., Hattori K., Ramachandran R., Feuerback F., Worgall S., Hackett N. R., Crystal R. G. 2001; Infection of endothelium with E1(−)E4(+), but not E1(−)E4(−), adenovirus gene transfer vectors enhances leukocyte adhesion and migration by modulation of ICAM-1, VCAM-1, CD34, and chemokine expression. Circ Res 88:903–910 [CrossRef]
     [Google Scholar]
  32. Raper S. E., Chirmule N., Lee F. S., Wivel N. A., Bagg A., Gao G. P., Wilson J. M., Batshaw M. L. 2003; Fatal systemic inflammatory response syndrome in a ornithine transcarbamylase deficient patient following adenoviral gene transfer. Mol Genet Metab 80:148–158 [CrossRef]
     [Google Scholar]
  33. Robertson M. J., Cochran K. J., Cameron C., Le J. M., Tantravahi R., Ritz J. 1996; Characterization of a cell line, NKL, derived from an aggressive human natural killer cell leukemia. Exp Hematol 24:406–415
     [Google Scholar]
  34. Rosen D. B., Bettadapura J., Alsharifi M., Mathew P. A., Warren H. S., Lanier L. L. 2005; Cutting edge: lectin-like transcript-1 is a ligand for the inhibitory human NKR-P1A receptor. J Immunol 175:7796–7799 [CrossRef]
     [Google Scholar]
  35. Routes J. M., Ryan S., Morris K., Takaki R., Cerwenka A., Lanier L. L. 2005; Adenovirus serotype 5 E1A sensitizes tumor cells to NKG2D-dependent NK cell lysis and tumor rejection. J Exp Med 202:1477–1482 [CrossRef]
     [Google Scholar]
  36. Ruzek M. C., Kavanagh B. F., Scaria A., Richards S. M., Garman R. D. 2002; Adenoviral vectors stimulate murine natural killer cell responses and demonstrate antitumor activities in the absence of transgene expression. Mol Ther 5:115–124 [CrossRef]
     [Google Scholar]
  37. Schnell M. A., Zhang Y., Tazelaar J., Gao G. P., Yu Q. C., Qian R., Chen S. J., Varnavski A. N., LeClair C. other authors 2001; Activation of innate immunity in nonhuman primates following intraportal administration of adenoviral vectors. Mol Ther 3:708–722 [CrossRef]
     [Google Scholar]
  38. Tomasec P., Braud V. M., Rickards C., Powell M. B., McSharry B. P., Gadola S., Cerundolo V., Borysiewicz L. K., McMichael A. J., Wilkinson G. W. 2000; Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287:1031 [CrossRef]
     [Google Scholar]
  39. Tomasec P., Wang E. C., Davison A. J., Vojtesek B., Armstrong M., Griffin C., McSharry B. P., Morris R. J., Llewellyn-Lacey S. other authors 2005; Downregulation of natural killer cell-activating ligand CD155 by human cytomegalovirus UL141. Nat Immunol 6:181–188
     [Google Scholar]
  40. Welte S. A., Sinzger C., Lutz S. Z., Singh-Jasuja H., Sampaio K. L., Eknigk U., Rammensee H. G., Steinle A. 2003; Selective intracellular retention of virally induced NKG2D ligands by the human cytomegalovirus UL16 glycoprotein. Eur J Immunol 33:194–203 [CrossRef]
     [Google Scholar]
  41. Wilkinson G. W., Akrigg A. 1992; Constitutive and enhanced expression from the CMV major IE promoter in a defective adenovirus vector. Nucleic Acids Res 20:2233–2239 [CrossRef]
     [Google Scholar]
  42. Wills M. R., Carmichael A. J., Maynard K., Xin J., Weekes M. P., Plachter B., Sissons J. G. 1996; The human cytotoxic T-lymphocyte (CTL) response to cytomegalovirus is dominated by structural protein pp65: frequency, specificity and T-cell receptor usage of pp65-specific CTL. J Virol 70:7569–7579
     [Google Scholar]
  43. Wills M. R., Ashiru O., Reeves M. B., Okecha G., Trowsdale J., Tomasec P., Wilkinson G. W., Sinclair J., Sissons J. G. 2005; Human cytomegalovirus encodes an MHC class I-like molecule (UL142) that functions to inhibit NK cell lysis. J Immunol 175:7457–7465 [CrossRef]
     [Google Scholar]
  44. Xu X., Zhang H. G., Liu Z. Y., Wu Q., Yang P. A., Sun S. H., Chen J., Hsu H. C., Mountz J. D. 2004; Defective clearance of adenovirus in IRF-1 mice associated with defects in NK and T cells but not macrophages. Scand J Immunol 60:89–99 [CrossRef]
     [Google Scholar]
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Adenovirus vector delivery stimulates natural killer cell recognition
J. Gen. Virol. 88, 1103 (2007); https://doi.org/10.1099/vir.0.82685-0
/content/journal/jgv/10.1099/vir.0.82685-0
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