Interleukin 18 coexpression during respiratory syncytial virus infection results in enhanced disease mediated by natural killer cells

Journal of Virology

Volumn 84, Issue 8, 2010, Pages 4073-4082

  Harker, James A ^a,d   Godlee, Alexandra ^a,e   Wahlsten, Jennifer L ^b   Lee, Debbie C P ^a   Thorne, Lucy G ^a   Sawant, Devika ^a   Tregoning, John S ^a,f   Caspi, Rachel R ^b   Bukreyev, Alexander ^c   Collins, Peter L ^c   Openshaw, Peter J M ^a  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b NATIONAL EYE INSTITUTE   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 18; MESSENGER RNA; RECOMBINANT VACCINE; RESPIRATORY SYNCYTIAL VIRUS VACCINE; VIRUS ANTIBODY;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CD8+ T LYMPHOCYTE; CELL ACTIVITY; CONTROLLED STUDY; CORRELATION ANALYSIS; DEPLETION; DISEASE SEVERITY; FEMALE; IMMUNE RESPONSE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RESPIRATORY TRACT INFECTION; T LYMPHOCYTE; VIRUS GENOME; VIRUS INFECTION; VIRUS LOAD; WEIGHT REDUCTION; ANIMAL; BAGG ALBINO MOUSE; BLOOD; GENETICS; IMMUNOLOGY; LEUKAPHERESIS; LUNG; PATHOLOGY; RESPIRATORY SYNCYTIAL VIRUS INFECTION; VIREMIA;

MURINAE; MUS; RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

ANIMALS; ANTIBODIES, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; INTERLEUKIN-18; KILLER CELLS, NATURAL; LEUKOCYTE REDUCTION PROCEDURES; LUNG; MICE; MICE, INBRED BALB C; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS VACCINES; RESPIRATORY SYNCYTIAL VIRUSES; VACCINES, SYNTHETIC; VIREMIA; WEIGHT LOSS;

EID: 77950509583     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02014-09     Document Type: Article

References (35)

1. Alwan, W. H., W. J. Kozlowska, and P. J. M. Openshaw. 1994. Distinct types of lung disease caused by functional subsets of antiviral T cells. J. Exp. Med. 179: 81-89.
2. Boelen, A., J. Kwakkel, M. Barends, L. de Rond, J. Dormans, and T. Kimman. 2002. Effect of lack of interleukin-4, interleukin-12, interleukin-18, or the interferon-gamma receptor on virus replication, cytokine response, and lung pathology during respiratory syncytial virus infection in mice. J. Med. Virol. 66: 552-560.
3. Bukreyev, A., I. M. Belyakov, J. A. Berzofsky, B. R. Murphy, and P. L. Collins. 2001. Granulocyte-macrophage colony-stimulating factor expressed by recombinant respiratory syncytial virus attenuates viral replication and increases the level of pulmonary antigen-presenting cells. J. Virol. 75: 12128-12140.
4. Bukreyev, A., I. M. Belyakov, G. A. Prince, K. C. Yim, K. K. Harris, J. A. Berzofsky, and P. L. Collins. 2005. Expression of interleukin-4 by recombinant respiratory syncytial virus is associated with accelerated inflammation and a nonfunctional cytotoxic T-lymphocyte response following primary infection but not following challenge with wild-type virus. J. Virol. 79: 9515-9526.
5. Bukreyev, A., E. Camargo, and P. L. Collins. 1996. Recovery of infectious respiratory syncytial virus expressing an additional, foreign gene. J. Virol. 70: 6634-6641.
6. Bukreyev, A., S. S. Whitehead, N. Bukreyeva, B. Murphy, and P. L. Collins. 1999. Interferon gamma expressed by a recombinant respiratory syncytial virus attenuates virus replication in mice without compromising immunogenicity. Proc. Natl. Acad. Sci. U. S. A. 96: 2367-2372.
7. Bukreyev, A., S. S. Whitehead, C. Prussin, B. R. Murphy, and P. L. Collins. 2000. Effect of coexpression of interleukin-2 by recombinant respiratory syncytial virus on virus replication, immunogenicity, and production of other cytokines. J. Virol. 74: 7151-7157.
8. Chaix, J., M. S. Tessmer, K. Hoebe, N. Fuseri, B. Ryffel, M. Dalod, L. Alexopoulou, B. Beutler, L. Brossay, E. Vivier, and T. Walzer. 2008. Cutting edge: priming of NK cells by IL-18. J. Immunol. 181: 1627-1631.
9. Collins, P. L., and B. S. Graham. 2008. Viral and host factors in human respiratory syncytial virus pathogenesis. J. Virol. 82: 2040-2055.
10. Collins, P. L., M. G. Hill, E. Camargo, H. Grosfeld, R. M. Chanock, and B. R. Murphy. 1995. Production of infectious human respiratory syncytial virus from cloned cDNA confirms an essential role for the transcription elongation factor from the 5' proximal open reading frame of the M2 mRNA in gene expression and provides a capability for vaccine development. Proc. Natl. Acad. Sci. U. S. A. 92: 11563-11567.
11. Culley, F. J., J. Pollott, and P. J. Openshaw. 2002. Age at first viral infection determines the pattern of T cell-mediated disease during reinfection in adulthood. J. Exp. Med. 196: 1381-1386.
12. Graham, B. S., L. A. Bunton, P. F. Wright, and D. T. Karzon. 1991. Role of T lymphocyte subsets in the pathogenesis of primary infection and rechallenge with respiratory syncytial virus in mice. J. Clin. Investig. 88: 1026-1033.
13. Harker, J., A. Bukreyev, P. L. Collins, B. Wang, P. J. Openshaw, and J. S. Tregoning. 2007. Virally delivered cytokines alter the immune response to future lung infections. J. Virol. 81: 13105-13111.
14. Hayakawa, Y., and M. J. Smyth. 2006. CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J. Immunol. 176: 1517-1524.
15. Kohno, K., J. Kataoka, T. Ohtsuki, Y. Suemoto, I. Okamoto, M. Usui, M. Ikeda, and M. Kurimoto. 1997. IFN-gamma-inducing factor (IGIF) is a costimulatory factor on the activation of Th1 but not Th2 cells and exerts its effect independently of IL-12. J. Immunol. 158: 1541-1550.
16. Lee, S. H., K. S. Kim, N. Fodil-Cornu, S. M. Vidal, and C. A. Biron. 2009. Activating receptors promote NK cell expansion for maintenance, IL-10 production, and CD8 T cell regulation during viral infection. J. Exp. Med. 206: 2235-2251.
17. Legg, J. P., I. R. Hussain, J. A. Warner, S. L. Johnston, and J. O. Warner. 2003. Type 1 and type 2 cytokine imbalance in acute respiratory syncytial virus bronchiolitis. Am. J. Respir. Crit. Care Med. 168: 633-639.
18. Liu, B., I. Mori, M. J. Hossain, L. Dong, K. Takeda, and Y. Kimura. 2004. Interleukin-18 improves the early defence system against influenza virus infection by augmenting natural killer cell-mediated cytotoxicity. J. Gen. Virol. 85: 423-428.
19. Okamoto, M., S. Kato, K. Oizumi, M. Kinoshita, Y. Inoue, K. Hoshino, S. Akira, A. N. McKenzie, H. A. Young, and T. Hoshino. 2002. Interleukin 18 (IL-18) in synergy with IL-2 induces lethal lung injury in mice: a potential role for cytokines, chemokines, and natural killer cells in the pathogenesis of interstitial pneumonia. Blood 99: 1289-1298.
20. Okamura, H., H. Tsutsi, T. Komatsu, M. Yutsudo, A. Hakura, T. Tanimoto, K. Torigoe, T. Okura, Y. Nukada, K. Hattori, et. al. 1995. Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature 378: 88-91.
21. Openshaw, P. J., and J. S. Tregoning. 2005. Immune responses and disease enhancement during respiratory syncytial virus infection. Clin. Microbiol. Rev. 18: 541-555.
22. Pribul, P. K., J. Harker, B. Wang, H. Wang, J. S. Tregoning, J. Schwarze, and P. J. Openshaw. 2008. Alveolar macrophages are a major determinant of early responses to viral lung infection but do not influence subsequent disease development. J. Virol. 82: 4441-4448.
23. Puthothu, B., M. Krueger, J. Forster, J. Heinze, M. Weckmann, and A. Heinzmann. 2007. Interleukin (IL)-18 polymorphism 133C/G is associated with severe respiratory syncytial virus infection. Pediatr. Infect. Dis. J. 26: 1094-1098.
24. Reading, P. C., P. G. Whitney, D. P. Barr, M. Wojtasiak, J. D. Mintern, J. Waithman, and A. G. Brooks. 2007. IL-18, but not IL-12, regulates NK cell activity following intranasal herpes simplex virus type 1 infection. J. Immunol. 179: 3214-3221.
25. Robinson, D., K. Shibuya, A. Mui, F. Zonin, E. Murphy, T. Sana, S. B. Hartley, S. Menon, R. Kastelein, F. Bazan, and A. O'Garra. 1997. IGIF does not drive Th1 development but synergizes with IL-12 for interferon-gamma production and activates IRAK and NFkappaB. Immunity 7: 571-581.
26. Takeda, K., H. Tsutsui, T. Yoshimoto, O. Adachi, N. Yoshida, T. Kishimoto, H. Okamura, K. Nakanishi, and S. Akira. 1998. Defective NK cell activity and Th1 response in IL-18-deficient mice. Immunity 8: 383-390.
27. Tregoning, J. S., and J. Schwarze. 2010. Respiratory viral infections in infancy: causes, clinical symptoms, virology, and immunology. Clin. Microbiol. Rev. 23: 74-98.
28. Tregoning, J. S., Y. Yamaguchi, J. Harker, B. Wang, and P. J. Openshaw. 2008. The role of T cells in the enhancement of respiratory syncytial virus infection severity during adult reinfection of neonatally sensitized mice. J. Virol. 82: 4115-4124.
29. Vivier, E., E. Tomasello, M. Baratin, T. Walzer, and S. Ugolini. 2008. Functions of natural killer cells. Nat. Immunol. 9: 503-510.
30. Wang, Y., G. Chaudhri, R. J. Jackson, and G. Karupiah. 2009. IL-12p40 and IL-18 play pivotal roles in orchestrating the cell-mediated immune response to a poxvirus infection. J. Immunol. 183: 3324-3331.
31. Wheelock, E. F. 1965. Interferon-like virus-inhibitor induced in human leukocytes by phytohemagglutinin. Science 149: 310-311.
32. Xu, D., W. L. Chan, B. P. Leung, D. Hunter, K. Schulz, R. W. Carter, I. B. McInnes, J. H. Robinson, and F. Y. Liew. 1998. Selective expression and functions of interleukin 18 receptor on T helper (Th) type 1 but not Th2 cells. J. Exp. Med. 188: 1485-1492. (Pubitemid 28489585)
33. Yoshimoto, T., H. Mizutani, H. Tsutsui, N. Noben-Trauth, K. Yamanaka, M. Tanaka, S. Izumi, H. Okamura, W. E. Paul, and K. Nakanishi. 2000. IL-18 induction of IgE: dependence on CD4+ T cells, IL-4 and STAT6. Nat. Immunol. 1: 132-137.
34. Yoshimoto, T., H. Okamura, Y. I. Tagawa, Y. Iwakura, and K. Nakanishi. 1997. Interleukin 18 together with interleukin 12 inhibits IgE production by induction of interferon-gamma production from activated B cells. Proc. Natl. Acad. Sci. U. S. A. 94: 3948-3953.
35. Yoshimoto, T., H. Tsutsui, K. Tominaga, K. Hoshino, H. Okamura, S. Akira, W. E. Paul, and K. Nakanishi. 1999. IL-18, although antiallergic when administered with IL-12, stimulates IL-4 and histamine release by basophils. Proc. Natl. Acad. Sci. U. S. A. 96: 13962-13966.