Adenovirus DNA polymerase is recognized by human CD8+ T cells

Journal of General Virology

Volumn 90, Issue 1, 2009, Pages 84-94

  Joshi, Amita ^a   Tang, Jie ^a   Kuzma, Melanie ^a   Wagner, John ^a   Mookerjee, Bijoyesh ^a   Filicko, Joanne ^a   Carabasi, Matthew ^a   Flomenberg, Neal ^a   Flomenberg, Phyllis ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIDOFOVIR; DNA BINDING PROTEIN; DNA POLYMERASE; EPITOPE; GAMMA INTERFERON; HLA A2 ANTIGEN; PEPTIDE DERIVATIVE; VIRUS ENZYME; DNA DIRECTED DNA POLYMERASE; VIRUS PROTEIN;

ADENOVIRUS; ADENOVIRUS INFECTION; ADULT; AGED; ANTIGEN SPECIFICITY; ARTICLE; CASE REPORT; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; FEMALE; HUMAN; HUMAN CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN TARGETING; T LYMPHOCYTE ACTIVATION; VIREMIA; VIRUS CELL INTERACTION; CYTOTOXICITY TEST; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; SECRETION; T LYMPHOCYTE SUBPOPULATION;

ADENOVIRIDAE; MIRIDAE;

ADENOVIRIDAE; ADULT; CD8-POSITIVE T-LYMPHOCYTES; CYTOTOXICITY TESTS, IMMUNOLOGIC; DNA-BINDING PROTEINS; DNA-DIRECTED DNA POLYMERASE; HUMANS; INTERFERON-GAMMA; LYMPHOCYTE ACTIVATION; T-LYMPHOCYTE SUBSETS; VIRAL NONSTRUCTURAL PROTEINS;

EID: 59849104551     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.002493-0     Document Type: Article

References (58)

1. Bennett, E. M., Bennink, J. R., Yewdell, J. W. & Brodsky, F. M. (1999). Cutting edge: adenovirus E19 has two mechanisms for affecting class I MHC expression. J Immunol 162, 5049-5052.
2. Bennink, J. R., Yewdell, J. W. & Gerhard, W. (1982). A viral polymerase involved in recognition of influenza virus-infected cells by a cytotoxic T-cell clone. Nature 296, 75-76.
3. Bordigoni, P., Carret, A. S., Venard, V., Witz, F. & Le Faou, A. (2001). Treatment of adenovirus infections in patients undergoing allogeneic hematopoietic stem cell transplantation. Clin Infect Dis 32, 1290-1297.
4. Bunde, T., Kirchner, A., Hoffmeister, B., Habedank, D., Hetzer, R., Cherepnev, G., Proesch, S., Reinke, P., Volk, H. D. & other authors (2005). Protection from cytomegalovirus after transplantation is correlated with immediate early 1-specific CD8 T cells. J Exp Med 201, 1031-1036.
5. Burgert, H. G. & Kvist, S. (1985). An adenovirus type 2 glycoprotein blocks cell surface expression of human histocompatibility class I antigens. Cell 41, 987-997.
6. + T cell responses in EBV infection. J Immunol 167, 4450-4457.
7. Chakrabarti, S., Collingham, K. E., Fegan, C. D., Pillay, D. & Milligan, D. W. (2000). Adenovirus infections following haematopoietic cell transplantation: is there a role for adoptive immunotherapy? Bone Marrow Transplant 26, 305-307.
8. Chakrabarti, S., Mautner, V., Osman, H., Collingham, K. E., Fegan, C. D., Klapper, P. E., Moss, P. A. & Milligan, D. W. (2002). Adenovirus infections following allogeneic stem cell transplantation: incidence and outcome in relation to graft manipulation, immunosuppression, and immune recovery. Blood 100, 1619-1627.
9. Cleghon, V., Piderit, A., Brough, D. E. & Klessig, D. F. (1993). Phosphorylation of the adenovirus DNA-binding protein and epitope mapping of monoclonal antibodies against it. Virology 197, 564-575.
10. Einsele, H., Roosnek, E., Rufer, N., Sinzger, C., Riegler, S., Loffler, J., Grigoleit, U., Moris, A., Rammensee, H. G. & other authors (2002). Infusion of cytomegalovirus (CMV)-specific T cells for the treatment of CMV infection not responding to antiviral chemotherapy. Blood 99, 3916-3922.
11. Feuchtinger, T., Matthes-Martin, S., Richard, C., Lion, T., Fuhrer, M., Hamprecht, K., Handgretinger, R., Peters, C., Schuster, F. & other authors (2006). Safe adoptive transfer of virus-specific T-cell immunity for the treatment of systemic adenovirus infection after allogeneic stem cell transplantation. Br J Haematol 134, 64-76.
12. Flomenberg, P., Babbitt, J., Drobyski, W. R., Ash, R. C., Carrigan, D. R., Sedmak, G. V., McAuliffe, T., Camitta, B., Horowitz, M. M. & Bunin, N. (1994). Increasing incidence of adenovirus didisease in bone marrow transplant recipients. J Infect Dis 169, 775-781.
13. Flomenberg, P., Piaskowski, V., Truitt, R. L. & Casper, J. T. (1995). Characterization of human proliferative T cell responses to adenovirus. J Infect Dis 171, 1090-1096.
14. + T-cell responses are not inhibited by E3-19K in the presence of gamma interferon. J Virol 70, 6314-6322.
15. Fuerst, T. R., Niles, E. G., Studier, F. W. & Moss, B. (1986). Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc Natl Acad Sci U S A 83, 8122-8126.
16. Green, M. & Wold, W. S. M. (1979). Human adenoviruses: growth, purification, and transfection assay. Methods Enzymol 58, 425-435.
17. Haveman, L. M., Bierings, M., Legger, E., Klein, M. R., de Jager, W., Otten, H. G., Albani, S., Kuis, W., Sette, A. & Prakken, B. J. (2006). Novel pan-DR-binding T cell epitopes of adenovirus induce pro-inflammatory cytokines and chemokines in healthy donors. Int Immunol 18, 1521-1529.
18. Heemskerk, B., Lankester, A. C., van Vreeswijk, T., Beersma, M. F., Claas, E. C., Veltrop-Duits, L. A., Kroes, A. C., Vossen, J. M., Schilham, M. W. & van Tol, M. J. (2005). Immune reconstitution and clearance of human adenovirus viremia in pediatric stem-cell recipients. J Infect Dis 191, 520-530.
19. + T cell clones recognizing endogenous antigen inhibit viral replication in vitro through cognate interaction. J Immunol 177, 8851-8859.
20. Horton, T. M., Ranheim, T. S., Aquino, L., Kusher, D. I., Saha, S. K., Ware, C. F., Wold, W. S. & Gooding, L. R. (1991). Adenovirus E3 14.7K protein functions in the absence of other adenovirus proteins to protect transfected cells from tumor necrosis factor cytolysis. J Virol 65, 2629-2639.
21. Hromas, R., Cornetta, K., Srour, E., Blanke, C. & Broun, E. R. (1994). Donor leukocyte infusion as therapy of life-threatening adenoviral infections after T-cell-depleted bone marrow transplantation. Blood 84, 1689-1690.
22. Ison, M. G. (2006). Adenovirus infections in transplant recipients. Clin Infect Dis 43, 331-339.
23. Izzedine, H., Launay-Vacher, V. & Deray, G. (2005). Antiviral drug-induced nephrotoxicity. Am J Kidney Dis 45, 804-817.
24. Jooss, K., Ertl, H. C. & Wilson, J. M. (1998). Cytotoxic T-lymphocyte target proteins and their major histocompatibility complex class I restriction in response to adenovirus vectors delivered to mouse liver. J Virol 72, 2945-2954.
25. Joung, I. & Engler, J. A. (1992). Mutations in two cysteine-histidinerich clusters in adenovirus type 2 DNA polymerase affect DNA binding. J Virol 66, 5788-5796.
26. Kast, W. M., Offringa, R., Peters, P. J., Voordouw, A. C., Meloen, R. H., van der Eb, A. J. & Melief, C. J. (1989). Eradication of adenovirus El-induced tumors by E1A-specific cytotoxic T lymphocytes. Cell 59, 603-614.
27. + T cells shapes the immunodominance hierarchy during boost vaccination. J Exp Med 204, 2187-2198.
28. Kitchingman, G. R. (1985). Sequence of the DNA-binding protein of a human subgroup E adenovirus (type 4): comparisons with subgroup A (type 12), subgroup B (type 7), and subgroup C (type 5). Virology 146, 90-101.
29. Knopf, C. W. (1998). Evolution of viral DNA-dependent DNA polymerases. Virus Genes 16, 47-58.
30. Kring, S. C. & Spindler, K. R. (1996). Lack of effect of mouse adenovirus type 1 infection on cell surface expression of major histocompatibility complex class I antigens. J Virol 70, 5495-5502.
31. La Rosa, A. M., Champlin, R. E., Mirza, N., Gajewski, J., Giralt, S., Rolston, K. V., Read, I., Jacobson, K., Kontoyiannis, D. & other authors (2001). Adenovirus infections in adult recipients of blood and marrow transplants. Clin Infect Dis 32, 871-876.
32. + T cells. Blood 104, 2432-2440.
33. Leen, A. M., Myers, G. D., Sili, U., Huls, M. H., Weiss, H., Leung, K. S., Carrum, G., Krance, R. A., Chang, C. C. & other authors (2006). Monoculture-derived T lymphocytes specific for multiple viruses expand and produce clinically relevant effects in immunocompromised individuals. Nat Med 12, 1160-1166.
34. Lichtenstein, D. L., Toth, K., Doronin, K., Tollefson, A. E. & Wold, W. S. (2004). Functions and mechanisms of action of the adenovirus E3 proteins. Int Rev Immunol 23, 75-111.
35. Liu, H., Naismith, J. H. & Hay, R. T. (2000). Identification of conserved residues contributing to the activities of adenovirus DNA polymerase. J Virol 74, 11681-11689.
36. Ljungman, P., Ribaud, P., Eyrich, M., Matthes-Martin, S., Einsele, H., Bleakley, M., Machaczka, M., Bierings, M., Bosi, A. & other authors (2003). Cidofovir for adenovirus infections after allogeneic hematopoietic stem cell transplantation: a survey by the Infectious Diseases Working Party of the European Group for Blood and Marrow Transplantation. Bone Marrow Transplant 31, 481-486.
37. McKelvey, T., Tang, A., Bett, A. J., Casimiro, D. R. & Chastain, M. (2004). T-cell response to adenovirus hexon and DNA-binding protein in mice. Gene Ther 11, 791-796.
38. Mizukoshi, E., Sidney, J., Livingston, B., Ghany, M., Hoofnagle, J. H., Sette, A, & Rehermann, B. (2004). Cellular immune responses to the hepatitis B virus polymerase. J Immunol 173, 5863-5871.
39. Muller, W. J., Levin, M. J., Shin, Y. K., Robinson, C., Quinones, R., Malcolm, J., Hild, E., Gao, D. & Giller, R. (2005). Clinical and in vitro evaluation of cidofovir for treatment of adenovirus infection in pediatric hematopoietic stem cell transplant recipients. Clin Infect Dis 41, 1812-1816.
40. Neofytos, D., Ojha, A., Mookerjee, B., Wagner, J., Filicko, J., Ferber, A., Dessain, S., Grosso, D., Brunner, J. & other authors (2007). Treatment of adenovirus disease in stem cell transplant recipients with cidofovir. Biol Blood Marrow Transplant 13, 74-81.
41. + T cell responses from healthy adults. Viral Immunol 14, 403-413.
42. + T-cell epitope. Hum Gene Ther 13, 1167-1178.
43. Papadopoulos, E. B., Ladanyl, M., Emanuel, D., Mackinnon, S., Boulad, F., Carabasi, M. H., Castro-Malaspina, H., Childs, B. H., Gillio, A. P. & Small, T. N. (1994). Infusions of donor leukocytes to treat Epstein-Barr virus-associated lymphoproliferative disorders after allogeneic bone marrow transplantation. N Engl J Med 330, 1185-1191.
44. Parker, K. C., Bednarek, M. A. & Coligan, J. E. (1994). Scheme for ranking potential HLA-A2 binding peptides based on independent binding of individual peptide side-chains. J Immunol 152, 163-175.
45. Rammensee, H. G., Friede, T. & Stevanović, S. (1995). MHC ligands and peptide motifs: first listing. Immunogenetics 41, 178-228.
46. Rooney, C. M., Smith, C. A., Ng, C. Y., Loftin, S. K., Sixbey, J. W., Gan, Y., Srivastava, D. K., Bowman, L. C., Krance, R. A. & other authors (1998). Infusion of cytotoxic T cells for the prevention and treatment of Epstein-Barr virus-induced lymphoma in allogeneic transplant recipients. Blood 92, 1549-1555.
47. Routes, J. M., Bellgrau, D., McGrory, W. J., Bautista, D. S., Graham, F. L. & Cook. J. L. (1991). Anti-adenovirus type 5 'cytotoxic T lymphocytes: immunodominant epitopes are encoded by, the E1A gene. J Virol 65, 1450-1457.
48. Shisler, J., Yang, C., Walter, B., Ware, C. F. & Gooding, L. R. (1997). The adenovirus E3-10.4K/14.5K complex mediates loss of cell surface Fas (CD95) and resistance to Fas-induced apoptosis. J Virol 71, 8299-8306.
49. Smith, C. A., Woodruff, L. S., Rooney, C. & Kitchingman, G. R. (1998). Extensive cross-reactivity of adenovirus-specific cytotoxic T cells. Hum Gene Ther 9, 1419-1427.
50. Sparer, T. E., Wynn, S. G., Clark D. J., Kaplan, J. M., Cardoza, L. M., Wadsworth, S. C., Smith, A. E. & Gooding, L. R. (1997). Generation of cytotoxic T lymphocytes against immunorecessive epitopes after multiple immunizations with adenovirus vectors is dependent on haplotype. J Virol 71, 2277-1284.
51. Tang, J., Olive, M., Champagne, K., Flomenberg, N., Eisenlohr, L., Hsu, S. & Flomenberg, P. (2004). Adenovirus hexon T-cell epitope is recognized by most adults and is restricted by HLA DP4, the most common class II allele. Gene Ther 11, 1408-1415.
52. + cytotoxic T cell responses to adenovirus capsid proteins. Virology 350, 312-322.
53. Tsomides, T. J., Aldovini, A., Johnson, R. P., Walker, B. D., Young, R. A. & Eisen, H. N. (1994). Naturally processed viral peptides recognized by cytotoxic T lymphocytes on cells chronically infected by human immunodeficiency virus type 1. J Exp Med 180, 1283-1293.
54. Vos, H. L., van der Lee, F. M., Reemst, A. M., van Loon, A. E. & Sussenbach, J. S. (1988). The genes encoding the DNA binding protein and the 23K protease of adenovirus types 40 and 41. Virology 163, 1-10.
55. Walter, E. A., Greenberg, P. D., Gilbert, M. J., Finch, R. J., Watanabe, K. S., Thomas, E. D. & Riddell, S. R. (1995). Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. N Engl J Med 333, 1038-1044.
56. Wysocka, M., Eisenlohr, L C., Otvos, L., Jr, Horowitz, D., Yewdell, J. W., Bennink, J. R. & Hackett, C. J. (1994). Identification of overlapping class I and class II H-2d restricted T cell determinants of influenza virus N1 neuraminidase that require infectious virus for presentation. Virology 201, 86-94.
57. Yang, S. Y., Milford, E., Hammerling, U. & Dupont B. (1989). Description of the reference panel of B-lymphoblastoid cell lines for factors of the HLA system: the B-cell line panel designed for the Tenth International Histocompatibility Workshop. In Immunobiology of HLA, vol. I: Histocompatibility Testing 1987, pp. 11-19. Edited by B. Dupont. New York. Springer-Verlag.
58. Yusuf, U., Hale, G. A., Carr, J., Gu, Z., Benaim, E., Woodard, P., Kasow, K. A., Horwitz, E. M., Leung, W. & other authors (2006). Cidofovir for the treatment of adenoviral infection in pediatric hematopoietic stem cell transplant patients. Transplantation 81, 1398-1404.