Polyinosinic-polycytidylic acid treatment of Friend retrovirus-infected mice improves functional properties of virus-specific T cells and prevents virus-induced disease

Journal of Immunology

Volumn 185, Issue 10, 2010, Pages 6179-6189

  Gibbert, Kathrin ^a   Dietze, Kirsten K ^a   Zelinskyy, Gennadiy ^a   Lang, Karl S ^b   Barchet, Winfried ^c   Kirschning, Carsten J ^a   Dittmer, Ulf ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; INTERLEUKIN 12P70; INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; POLYINOSINIC POLYCYTIDYLIC ACID; RANTES; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG MECHANISM; ERYTHROLEUKEMIA; FEMALE; FRIEND LEUKEMIA VIRUS; IMMUNE RESPONSE; IMMUNOTHERAPY; INTERFERON INDUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RETROVIRUS INFECTION; RNA ISOLATION; SPLENOMEGALY; TREATMENT OUTCOME; VIRUS LOAD; VIRUS REPLICATION;

ANIMALS; ANTIVIRAL AGENTS; FEMALE; FRIEND MURINE LEUKEMIA VIRUS; INTERFERON TYPE I; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; POLY I-C; RETROVIRIDAE INFECTIONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES; TUMOR VIRUS INFECTIONS; VIRAL LOAD;

EID: 78650641138     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000858     Document Type: Article

References (82)

1. Stetson, D. B., and R. Medzhitov. 2006. Type I interferons in host defense. Immunity 25:373-381.
2. Gitlin, L., W. Barchet, S. Gilfillan, M. Cella, B. Beutler, R. A. Flavell, M. S. Diamond, and M. Colonna. 2006. Essential role of mda-5 in type I IFN responses to polyriboinosinic: polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. USA 103:8459-8464.
3. de Veer, M. J., M. Holko, M. Frevel, E. Walker, S. Der, J. M. Paranjape, R. H. Silverman, and B. R. Williams. 2001. Functional classification of interferonstimulated genes identified using microarrays. J. Leukoc. Biol. 69:912-920.
4. Meurs, E., K. Chong, J. Galabru, N. S. Thomas, I. M. Kerr, B. R. Williams, and A. G. Hovanessian. 1990. Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon. Cell 62:379-390.
5. Zhou, A., B. A. Hassel, and R. H. Silverman. 1993. Expression cloning of 2-5A-dependent RNAase: a uniquely regulated mediator of interferon action. Cell 72:753-765.
6. Walzer, T., M. Dalod, S. H. Robbins, L. Zitvogel, and E. Vivier. 2005. Naturalkiller cells and dendritic cells: "l'union fait la force". Blood 106:2252-2258.
7. Kolumam, G. A., S. Thomas, L. J. Thompson, J. Sprent, and K. Murali-Krishna. 2005. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J. Exp. Med. 202:637-650.
8. Le Bon, A., N. Etchart, C. Rossmann, M. Ashton, S. Hou, D. Gewert, P. Borrow, and D. F. Tough. 2003. Cross-priming of CD8+ T cells stimulated by virusinduced type I interferon. Nat. Immunol. 4:1009-1015.
9. Haller, O., G. Kochs, and F. Weber. 2006. The interferon response circuit: induction and suppression by pathogenic viruses. Virology 344:119-130.
10. Perdiguero, B., and M. Esteban. 2009. The interferon system and vaccinia virus evasion mechanisms. J. Interferon Cytokine Res. 29:581-598.
11. García-Sastre, A. 2001. Inhibition of interferon-mediated antiviral responses by influenza A viruses and other negative-strand RNA viruses. Virology 279:375-384.
12. García-Sastre, A., A. Egorov, D. Matassov, S. Brandt, D. E. Levy, J. E. Durbin, P. Palese, and T. Muster. 1998. Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252:324-330.
13. Graff, J. W., K. Ettayebi, and M. E. Hardy. 2009. Rotavirus NSP1 inhibits NFkappaB activation by inducing proteasome-dependent degradation of beta-TrCP: a novel mechanism of IFN antagonism. PLoS Pathog. 5: e1000280.
14. Brzózka, K., S. Finke, and K. K. Conzelmann. 2005. Identification of the rabies virus alpha/beta interferon antagonist: phosphoprotein P interferes with phosphorylation of interferon regulatory factor 3. J. Virol. 79:7673-7681.
15. Hahn, A. M., L. E. Huye, S. Ning, J. Webster-Cyriaque, and J. S. Pagano. 2005. Interferon regulatory factor 7 is negatively regulated by the Epstein-Barr virus immediate-early gene, BZLF-1. J. Virol. 79:10040-10052.
16. Yokota, S., N. Yokosawa, T. Okabayashi, T. Suzutani, S. Miura, K. Jimbow, and N. Fujii. 2004. Induction of suppressor of cytokine signaling-3 by herpes simplex virus type 1 contributes to inhibition of the interferon signaling pathway. J. Virol. 78:6282-6286.
17. Elia, A., K. G. Laing, A. Schofield, V. J. Tilleray, and M. J. Clemens. 1996. Regulation of the double-stranded RNA-dependent protein kinase PKR by RNAs encoded by a repeated sequence in the Epstein-Barr virus genome. Nucleic Acids Res. 24:4471-4478.
18. Bode, J. G., S. Ludwig, C. Ehrhardt, U. Albrecht, A. Erhardt, F. Schaper, P. C. Heinrich, and D. Häussinger. 2003. IFN-alpha antagonistic activity of HCV core protein involves induction of suppressor of cytokine signaling-3. FASEB J. 17:488-490.
19. Meylan, E., J. Curran, K. Hofmann, D. Moradpour, M. Binder, R. Bartenschlager, and J. Tschopp. 2005. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437:1167-1172.
20. Gale, M. J., Jr., M. J. Korth, and M. G. Katze. 1998. Repression of the PKR protein kinase by the hepatitis C virus NS5A protein: a potential mechanism of interferon resistance. Clin. Diagn. Virol. 10:157-162.
21. Keskinen, P., K. Melén, and I. Julkunen. 2002. Expression of HCV structural proteins impairs IFN-mediated antiviral response. Virology 299:164-171.
22. Melén, K., R. Fagerlund, M. Nyqvist, P. Keskinen, and I. Julkunen. 2004. Expression of hepatitis C virus core protein inhibits interferon-induced nuclear import of STATs. J. Med. Virol. 73:536-547.
23. Kitajewski, J., R. J. Schneider, B. Safer, S. M. Munemitsu, C. E. Samuel, B. Thimmappaya, and T. Shenk. 1986. Adenovirus VAI RNA antagonizes the antiviral action of interferon by preventing activation of the interferon-induced eIF-2 alpha kinase. Cell 45:195-200.
24. Leonard, G. T., and G. C. Sen. 1996. Effects of adenovirus E1A protein on interferon-signaling. Virology 224:25-33.
25. Look, D. C., W. T. Roswit, A. G. Frick, Y. Gris-Alevy, D. M. Dickhaus, M. J. Walter, and M. J. Holtzman. 1998. Direct suppression of Stat1 function during adenoviral infection. Immunity 9:871-880.
26. Kamga, I., S. Kahi, L. Develioglu, M. Lichtner, C. Marañón, C. Deveau, L. Meyer, C. Goujard, P. Lebon, M. Sinet, and A. Hosmalin. 2005. Type I interferon production is profoundly and transiently impaired in primary HIV-1 infection. J. Infect. Dis. 192:303-310.
27. Feldman, S., D. Stein, S. Amrute, T. Denny, Z. Garcia, P. Kloser, Y. Sun, N. Megjugorac, and P. Fitzgerald-Bocarsly. 2001. Decreased interferon-alpha production in HIV-infected patients correlates with numerical and functional deficiencies in circulating type 2 dendritic cell precursors. Clin. Immunol. 101:201-210.
28. Khatissian, E., M. G. Tovey, M. C. Cumont, V. Monceaux, P. Lebon, L. Montagnier, B. Hurtrel, and L. Chakrabarti. 1996. The relationship between the interferon alpha response and viral burden in primary SIV infection. AIDS Res. Hum. Retroviruses 12:1273-1278.
29. Gerlach, N., S. Schimmer, S. Weiss, U. Kalinke, and U. Dittmer. 2006. Effects of type I interferons on Friend retrovirus infection. J. Virol. 80:3438-3444.
30. Gerlach, N., S. Schimmer, S. Weiss, U. Kalinke, and U. Dittmer. 2007. Effects of type I interferons on Friend retrovirus infection [Erratum]. J. Virol. 81:6160.
31. Loré, K., M. R. Betts, J. M. Brenchley, J. Kuruppu, S. Khojasteh, S. Perfetto, M. Roederer, R. A. Seder, and R. A. Koup. 2003. Toll-like receptor ligands modulate dendritic cells to augment cytomegalovirus-and HIV-1-specific T cell responses. J. Immunol. 171:4320-4328.
32. Trapp, S., N. R. Derby, R. Singer, A. Shaw, V. G. Williams, S. G. Turville, J. W. Bess, Jr., J. D. Lifson, and M. Robbiani. 2009. Double-stranded RNA analog poly (I:C) inhibits human immunodeficiency virus amplification in dendritic cells via type I interferon-mediated activation of APOBEC3G. J. Virol. 83:884-895.
33. Lane, H. C., V. Davey, J. A. Kovacs, J. Feinberg, J. A. Metcalf, B. Herpin, R. Walker, L. Deyton, R. T. Davey, Jr., J. Falloon, et al. 1990. Interferon-alpha in patients with asymptomatic human immunodeficiency virus (HIV) infection. A randomized, placebo-controlled trial. Ann. Intern. Med. 112:805-811.
34. Kovacs, J. A., C. Bechtel, R. T. Davey, Jr., J. Falloon, M. A. Polis, R. E. Walker, J. A. Metcalf, V. Davey, S. C. Piscitelli, M. Baseler, et al. 1996. Combination therapy with didanosine and interferon-alpha in human immunodeficiency virusinfected patients: results of a phase I/II trial. J. Infect. Dis. 173:840-848.
35. Hardy, G. A., S. F. Sieg, B. Rodriguez, W. Jiang, R. Asaad, M. M. Lederman, and C. V. Harding. 2009. Desensitization to type I interferon in HIV-1 infection correlates with markers of immune activation and disease progression. Blood 113:5497-5505.
36. Alexopoulou, L., A. C. Holt, R. Medzhitov, and R. A. Flavell. 2001. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413:732-738.
37. Kato, H., O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, K. Matsui, S. Uematsu, A. Jung, T. Kawai, K. J. Ishii, et al. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101-105.
38. Salem, M. L., S. A. El-Naggar, A. Kadima, W. E. Gillanders, and D. J. Cole. 2006. The adjuvant effects of the toll-like receptor 3 ligand polyinosiniccytidylic acid poly (I:C) on antigen-specific CD8+ T cell responses are partially dependent on NK cells with the induction of a beneficial cytokine milieu. Vaccine 24:5119-5132.
39. Ashkar, A. A., X. D. Yao, N. Gill, D. Sajic, A. J. Patrick, and K. L. Rosenthal. 2004. Toll-like receptor (TLR)-3, but not TLR4, agonist protects against genital herpes infection in the absence of inflammation seen with CpG DNA. J. Infect. Dis. 190:1841-1849.
40. Field, A. K., A. A. Tytell, G. P. Lampson, and M. R. Hilleman. 1967. Inducers of interferon and host resistance. II. Multistranded synthetic polynucleotide complexes. Proc. Natl. Acad. Sci. USA 58:1004-1010.
41. Herbst-Kralovetz, M. M., and R. B. Pyles. 2006. Quantification of poly (I:C) - mediated protection against genital herpes simplex virus type 2 infection. J. Virol. 80:9988-9997.
42. Malmgaard, L., J. Melchjorsen, A. G. Bowie, S. C. Mogensen, and S. R. Paludan. 2004. Viral activation of macrophages through TLR-dependent and-independent pathways. J. Immunol. 173:6890-6898.
43. Nazli, A., X. D. Yao, M. Smieja, K. L. Rosenthal, A. A. Ashkar, and C. Kaushic. 2009. Differential induction of innate anti-viral responses by TLR ligands against Herpes simplex virus, type 2, infection in primary genital epithelium of women. Antiviral Res. 81:103-112.
44. Kabat, D. 1989. Molecular biology of Friend viral erythroleukemia. Curr. Top. Microbiol. Immunol. 148:1-42.
45. Miyazawa, M., J. Nishio, and B. Chesebro. 1992. Protection against Friend retrovirus-induced leukemia by recombinant vaccinia viruses expressing the gag gene. J. Virol. 66:4497-4507.
46. Müller, U., U. Steinhoff, L. F. Reis, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264:1918-1921.
47. Honda, K., S. Sakaguchi, C. Nakajima, A. Watanabe, H. Yanai, M. Matsumoto, T. Ohteki, T. Kaisho, A. Takaoka, S. Akira, et al. 2003. Selective contribution of IFN-alpha/beta signaling to the maturation of dendritic cells induced by doublestranded RNA or viral infection. Proc. Natl. Acad. Sci. USA 100:10872-10877.
48. Werts, C., R. I. Tapping, J. C. Mathison, T. H. Chuang, V. Kravchenko, I. Saint Girons, D. A. Haake, P. J. Godowski, F. Hayashi, A. Ozinsky, et al. 2001. Leptospiral lipopolysaccharide activates cells through a TLR2-dependent mechanism. Nat. Immunol. 2:346-352.
49. Hasenkrug, K. J., D. M. Brooks, M. N. Robertson, R. V. Srinivas, and B. Chesebro. 1998. Immunoprotective determinants in friend murine leukemia virus envelope protein. Virology 248:66-73.
50. Dittmer, U., D. M. Brooks, and K. J. Hasenkrug. 1998. Characterization of a liveattenuated retroviral vaccine demonstrates protection via immune mechanisms. J. Virol. 72:6554-6558.
51. Stromnes, I. M., U. Dittmer, T. N. Schumacher, K. Schepers, R. J. Messer, L. H. Evans, K. E. Peterson, B. Race, and K. J. Hasenkrug. 2002. Temporal effects of gamma interferon deficiency on the course of Friend retrovirus infection in mice. J. Virol. 76:2225-2232.
52. Chen, W., H. Qin, B. Chesebro, and M. A. Cheever. 1996. Identification of a gagencoded cytotoxic T-lymphocyte epitope from FBL-3 leukemia shared by Friend, Moloney, and Rauscher murine leukemia virus-induced tumors. J. Virol. 70:7773-7782.
53. Shimizu, T., H. Uenishi, Y. Teramura, M. Iwashiro, K. Kuribayashi, H. Tamamura, N. Fujii, and H. Yamagishi. 1994. Fine structure of a virus-encoded helper T-cell epitope expressed on FBL-3 tumor cells. J. Virol. 68:7704-7708.
54. Zelinskyy, G., A. R. Kraft, S. Schimmer, T. Arndt, and U. Dittmer. 2006. Kinetics of CD8+ effector T cell responses and induced CD4+ regulatory T cell responses during Friend retrovirus infection. Eur. J. Immunol. 36:2658-2670.
55. He, H., R. J. Messer, S. Sakaguchi, G. Yang, S. J. Robertson, and K. J. Hasenkrug. 2004. Reduction of retrovirus-induced immunosuppression by in vivo modulation of T cells during acute infection. J. Virol. 78:11641-11647.
56. Peterson, K. E., M. Iwashiro, K. J. Hasenkrug, and B. Chesebro. 2000. Major histocompatibility complex class I gene controls the generation of gamma interferon-producing CD4 (+) and CD8 (+) T cells important for recovery from friend retrovirus-induced leukemia. J. Virol. 74:5363-5367.
57. Zelinskyy, G., K. K. Dietze, Y. P. Hüsecken, S. Schimmer, S. Nair, T. Werner, K. Gibbert, O. Kershaw, A. D. Gruber, T. Sparwasser, and U. Dittmer. 2009. The regulatory T-cell response during acute retroviral infection is locally defined and controls the magnitude and duration of the virus-specific cytotoxic T-cell response. Blood 114:3199-3207.
58. Dittmer, U., B. Race, K. E. Peterson, I. M. Stromnes, R. J. Messer, and K. J. Hasenkrug. 2002. Essential roles for CD8+ T cells and gamma interferon in protection of mice against retrovirus-induced immunosuppression. J. Virol. 76:450-454.
59. Zelinskyy, G., S. Balkow, S. Schimmer, T. Werner, M. M. Simon, and U. Dittmer. 2007. The level of friend retrovirus replication determines the cytolytic pathway of CD8+ T-cell-mediated pathogen control. J. Virol. 81:11881-11890.
60. Zelinskyy, G., S. J. Robertson, S. Schimmer, R. J. Messer, K. J. Hasenkrug, and U. Dittmer. 2005. CD8+ T-cell dysfunction due to cytolytic granule deficiency in persistent Friend retrovirus infection. J. Virol. 79:10619-10626.
61. Ghosh, S. K., J. Kusari, S. K. Bandyopadhyay, H. Samanta, R. Kumar, and G. C. Sen. 1991. Cloning, sequencing, and expression of two murine 2′-5′-oligoadenylate synthetases. Structure-function relationships. J. Biol. Chem. 266:15293-15299.
62. Tough, D. F. 2004. Type I interferon as a link between innate and adaptive immunity through dendritic cell stimulation. Leuk. Lymphoma 45:257-264.
63. Nguyen, K. B., T. P. Salazar-Mather, M. Y. Dalod, J. B. Van Deusen, X. Q. Wei, F. Y. Liew, M. A. Caligiuri, J. E. Durbin, and C. A. Biron. 2002. Coordinated and distinct roles for IFN-alpha beta, IL-12, and IL-15 regulation of NK cell responses to viral infection. J. Immunol. 169:4279-4287.
64. Curtsinger, J. M., J. O. Valenzuela, P. Agarwal, D. Lins, and M. F. Mescher. 2005. Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J. Immunol. 174:4465-4469.
65. Neumann, A. U., N. P. Lam, H. Dahari, D. R. Gretch, T. E. Wiley, T. J. Layden, and A. S. Perelson. 1998. Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-alpha therapy. Science 282:103-107.
66. Feld, J. J., and J. H. Hoofnagle. 2005. Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 436:967-972.
67. Gerlach, N., K. Gibbert, C. Alter, S. Nair, G. Zelinskyy, C. M. James, and U. Dittmer. 2009. Anti-retroviral effects of type I IFN subtypes in vivo. Eur. J. Immunol. 39:136-146.
68. Seder, R. A., P. A. Darrah, and M. Roederer. 2008. T-cell quality in memory and protection: implications for vaccine design. Nat. Rev. Immunol. 8:247-258.
69. Darrah, P. A., D. T. Patel, P. M. de Luca, R. W. Lindsay, D. F. Davey, B. J. Flynn, S. T. Hoff, P. Andersen, S. G. Reed, S. L. Morris, et al. 2007. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 13:843-850.
70. Nair, S. R., G. Zelinskyy, S. Schimmer, N. Gerlach, G. Kassiotis, and U. Dittmer. 2010. Mechanisms of control of acute Friend virus infection by CD4+ T helper cells and their functional impairment by regulatory T cells. J. Gen. Virol. 91:440-451.
71. Parronchi, P., M. de Carli, R. Manetti, C. Simonelli, S. Sampognaro, M. P. Piccinni, D. Macchia, E. Maggi, G. del Prete, and S. Romagnani. 1992. IL-4 and IFN (alpha and gamma) exert opposite regulatory effects on the development of cytolytic potential by Th1 or Th2 human T cell clones. J. Immunol. 149:2977-2983.
72. Aman, M. J., T. Tretter, I. Eisenbeis, G. Bug, T. Decker, W. E. Aulitzky, H. Tilg, C. Huber, and C. Peschel. 1996. Interferon-alpha stimulates production of interleukin-10 in activated CD4+ T cells and monocytes. Blood 87:4731-4736.
73. Brinkmann, V., T. Geiger, S. Alkan, and C. H. Heusser. 1993. Interferon alpha increases the frequency of interferon gamma-producing human CD4+ T cells. J. Exp. Med. 178:1655-1663.
74. Schandené, L., E. Cogan, A. Crusiaux, and M. Goldman. 1997. Interferon-alpha upregulates both interleukin-10 and interferon-gamma production by human CD4+ T cells. Blood 89:1110-1111.
75. Havenar-Daughton, C., G. A. Kolumam, and K. Murali-Krishna. 2006. Cutting edge: The direct action of type I IFN on CD4 T cells is critical for sustaining clonal expansion in response to a viral but not a bacterial infection. J. Immunol. 176:3315-3319.
76. Kraft, A. R., T. Arndt, K. J. Hasenkrug, and U. Dittmer. 2005. Effective treatment of retrovirus-induced suppression of antibody responses with CpG oligodeoxynucleotides. J. Gen. Virol. 86:3365-3368.
77. Kraft, A. R., F. Krux, S. Schimmer, C. Ohlen, P. D. Greenberg, and U. Dittmer. 2007. CpG oligodeoxynucleotides allow for effective adoptive T-cell therapy in chronic retroviral infection. Blood 109:2982-2984.
78. McCartney, S., W. Vermi, S. Gilfillan, M. Cella, T. L. Murphy, R. D. Schreiber, K. M. Murphy, and M. Colonna. 2009. Distinct and complementary functions of MDA5 and TLR3 in poly (I:C)-mediated activation of mouse NK cells. J. Exp. Med. 206:2967-2976.
79. Ngoi, S. M., M. G. Tovey, and A. T. Vella. 2008. Targeting poly (I:C) to the TLR3-independent pathway boosts effector CD8 T cell differentiation through IFN-alpha/beta. J. Immunol. 181:7670-7680.
80. Kumar, H., S. Koyama, K. J. Ishii, T. Kawai, and S. Akira. 2008. Cutting edge: cooperation of IPS-1-and TRIF-dependent pathways in poly IC-enhanced antibody production and cytotoxic T cell responses. J. Immunol. 180:683-687.
81. Wang, Y., M. Cella, S. Gilfillan, and M. Colonna. 2010. Cutting edge: polyinosinic: polycytidylic acid boosts the generation of memory CD8 T cells through melanoma differentiation-associated protein 5 expressed in stromal cells. J. Immunol. 184:2751-2755.
82. Barchet, W., V. Wimmenauer, M. Schlee, and G. Hartmann. 2008. Accessing the therapeutic potential of immunostimulatory nucleic acids. Curr. Opin. Immunol. 20:389-395.