Aryl hydrocarbon receptor activation reduces dendritic cell function during influenza virus infection

Toxicological Sciences

Volumn 116, Issue 2, 2010, Pages 514-522

  Jin, Guang Bi ^a   Moore, Amanda J ^a   Head, Jennifer L ^a   Neumiller, Joshua J ^b   Lawrence, B Paige ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Ah receptor; Dendritic cells; Influenza virus; Mice; TCDD

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; GAMMA INTERFERON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CELL ISOLATION; CELL MIGRATION; CELL STIMULATION; CONTROLLED STUDY; DENDRITIC CELL; DNA BINDING; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; IMMUNOMODULATION; IMMUNOREGULATION; INFLUENZA; INFLUENZA VIRUS; MEDIASTINUM LYMPH NODE; MOUSE; NONHUMAN; T LYMPHOCYTE ACTIVATION; ANIMAL; C57BL MOUSE; CELL MOTION; IMMUNOLOGY; LYMPH NODE; LYMPHOCYTE ACTIVATION; ORTHOMYXOVIRUS INFECTION; PHYSIOLOGY; TOXICITY;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; DENDRITIC CELLS; FEMALE; LYMPH NODES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; ORTHOMYXOVIRIDAE INFECTIONS; RECEPTORS, ARYL HYDROCARBON; TETRACHLORODIBENZODIOXIN;

EID: 77955071099     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq153     Document Type: Article

References (60)

1. Bankoti, J., Burnett, A., Navarro, S., Miller, A. K., Rase, B., and Shepherd, D. M. (2010). Effects of TCDD on the fate of naive dendritic cells. Toxicol. Sci. 115, 422-434.
2. Belz, G. T., Bedoui, S., Kupresanin, F., Carbone, F. R., and Heath, W. R. (2007). Minimal activation of memory CD8+ T cell by tissue-derived dendritic cells favors the stimulation of naive CD8+ T cells. Nat. Immunol. 8, 1060-1066.
3. Belz, G. T., Smith, C. M., Kleinert, L., Reading, P., Brooks, A., Shortman, K., Carbone, F. R., and Heath, W. R. (2004). Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc. Natl. Acad. Sci. U.S.A. 101, 8670-8675.
4. Belz, G. T., Xie, W., and Doherty, P. C. (2001). Diversity of epitope and cytokine profiles for primary and secondary influenza a virus-specific CD8+ T cell responses. J. Immunol. 166, 4627-4633.
5. Brimnes, M. K., Bonifaz, L., Steinman, R. M., and Moran, T. M. (2003). Influenza virus-induced dendritic cell maturation is associated with the induction of strong T cell immunity to a co-administered, normally nonimmunogenic protein. J. Exp. Med. 198, 133-144.
6. Bunger, M. K., Glover, E., Moran, S. M., Walisser, J. A., Lahvis, G. P., Hsu, E. L., and Bradfield, C. A. (2008). Abnormal liver development and resistance to 2,3,7,8-tetrachlorodibenzo-p-dioxin toxicity in mice carrying a mutation in the DNA-binding domain of the aryl hydrocarbon receptor. Toxicol. Sci. 106, 83-92.
7. Celli, S., Garcia, Z., Beuneu, H., and Bousso, P. (2008). Decoding the dynamics of T cell-dendritic cell interactions in vivo. Immunol. Rev. 221, 182-187.
8. Croft, M., and Dubey, C. (1997). Accessory molecule and costimulation requirements for CD4 T cell response. Crit. Rev. Immunol. 17, 89-118.
9. Dallaire, F., Dewailly, E., Vezina, C., Muckle, G., Weber, J. P., Bruneau, S., and Ayotte, P. (2006). Effect of prenatal exposure to polychlorinated biphenyls on incidence of acute respiratory infections in preschool Inuit children. Environ. Health Perspect. 114, 1301-1305.
10. Esser, C. (2009). The immune phenotype of AhR null mouse mutants: not a simple mirror of xenobiotic receptor over-activation. Biochem. Pharmacol. 77, 597-607.
11. Flynn, K. J., Belz, G. T., Altman, J. D., Ahmed, R., Woodland, D. L., and Doherty, P. C. (1998). Virus-specific CD8+ T cells in primary and secondary influenza pneumonia. Immunity 8, 683-691.
12. Foy, T. M., Aruffo, A., Bajorath, J., Buhlmann, J. E., and Noelle, R. J. (1996). Immune regulation by CD40 and its ligand GP39. Annu. Rev. Immunol. 14, 591-617.
13. Fujii-Kuriyama, Y., and Mimura, J. (2005). Molecular mechanisms of AhR functions in the regulation of cytochrome P450 genes. Biochem. Biophys. Res. Commun. 338, 311-317.
14. Gasiewicz, T. A., Geiger, L. E., Rucci, G., and Neal, R. A. (1983). Distribution, excretion, and metabolism of 2,3,7,8-tetrachlorodibenzo-p-dioxin in C57BL/6J, DBA/2J, and B6D2F1/J mice. Drug Metab. Dispos. 11, 397-403.
15. Grayson, M. H., and Holtzman, M. J. (2007). Emerging role of dendritic cells in respiratory viral infection. J. Mol. Med. 85, 1057-1068.
16. Hauben, E., Gregori, S., Draghici, E., Migliavacca, B., Olivieri, S., Woisetschlager, M., and Roncarolo, M. G. (2008). Activation of the aryl hydrocarbon receptor promotes allograft-specific tolerance through direct and dendritic cell-mediated effects on regulatory T cells. Blood 112, 1214-1222.
17. Heilmann, C., Grandjean, P., Weihe, P., Nielsen, F., and Budtz-Jorgensen, E. (2006). Reduced antibody responses to vaccinations in children exposed to polychlorinated biphenyls. PLoS Med. 3, e311.
18. Henrickson, S. E., Mempel, T. R., Mazo, I. B., Liu, B., Artyomov, M. N., Zheng, H., Peixoto, A., Flynn, M. P., Senman, B., Junt, T., et al. (2008). T cell sensing of antigen dose governs interactive behavior with dendritic cells and sets a threshold for T cell activation. Nat. Immunol. 9, 282-291.
19. Hwang, J. A., Lee, J. A., Cheong, S. W., Youn, H. J., and Park, J. H. (2007). Benzo(a)pyrene inhibits growth and functional differentiation of mouse bone marrow-derived dendritic cells. Downregulation of RelB and eIF3 p170 by benzo(a)pyrene. Toxicol. Lett. 169, 82-90.
20. Kerkvliet, N. I. (2009). AHR-mediated immunomodulation: the role of altered gene transcription. Biochem. Pharmacol. 77, 746-760.
21. Kerkvliet, N. I., Baecher-Steppan, L., Shepherd, D. M., Oughton, J. A., Vorderstrasse, B. A., and DeKrey, G. K. (1996). Inhibition of TC-1 cytokine production, effector cytotoxic T lymphocyte development and alloantibody production by 2,3,7,8-tetrachlorodibenzo-p-dioxin. J. Immunol. 157, 2310-2319.
22. Kim, T. S., and Braciale, T. J. (2009). Respiratory dendritic cell subsets differ in their capacity to support the induction of virus-specific cytotoxic CD8+ T cell responses. PLoS One 4, e4204.
23. Kohlmeier, J. E., and Woodland, D. L. (2009). Immunity to respiratory viruses. Annu. Rev. Immunol. 27, 61-82.
24. Laupeze, B., Amiot, L., Sparfel, L., Le Ferrec, E., Fauchet, R., and Fardel, O. (2002). Polycyclic aromatic hydrocarbons affect functional differentiation and maturation of human monocyte-derived dendritic cells. J. Immunol. 168, 2652-2658.
25. Lawrence, B. P., Denison, M. S., Novak, H., Vorderstrasse, B. A., Harrer, N., Neruda, W., Reichel, C., and Woisetschlager, M. (2008). Activation of the aryl hydrocarbon receptor is essential for mediating the anti-inflammatory effects of a novel low-molecular-weight compound. Blood 112, 1158-1165.
26. Lawrence, B. P., Roberts, A. D., Neumiller, J. J., Cundiff, J. A., and Woodland, D. L. (2006). Aryl hydrocarbon receptor activation impairs the priming but not the recall of influenza virus-specific CD8+ T cells in the lung. J. Immunol. 177, 5819-5828.
27. Lawrence, B. P., and Vorderstrasse, B. A. (2004). Activation of the aryl hydrocarbon receptor diminishes the memory response to homotypic influenza virus infection but does not impair host resistance. Toxicol. Sci. 79, 304-314.
28. Lawrence, C. W., Ream, R. M., and Braciale, T. J. (2005). Frequency, specificity, and sites of expansion of CD8+ T cells during primary pulmonary influenza virus infection. J. Immunol. 174, 5332-5340.
29. Lee, J. A., Hwang, J. A., Sung, H. N., Jeon, C. H., Gill, B. C., Youn, H. J., and Park, J. H. (2007). 2,3,7,8-Tetrachlorodibenzo-p-dioxin modulates functional differentiation of mouse bone marrow-derived dendritic cells. Downregulation of RelB by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol. Lett. 173, 31-40.
30. Legge, K. L., and Braciale, T. J. (2003). Accelerated migration of respiratory dendritic cells to the regional lymph nodes is limited to the early phase of pulmonary infection. Immunity 18, 265-277.
31. Macagno, A., Napolitani, G., Lanzavecchia, A., and Sallusto, F. (2007). Duration, combination and timing: the signal integration model of dendritic cell activation. Trends Immunol. 28, 227-233.
32. Mamalaki, C., Elliott, J., Norton, T., Yannoutsos, N., Townsend, A. R., Chandler, P., Simpson, E., and Kioussis, D. (1993). Positive and negative selection in transgenic mice expressing a T-cell receptor specific for influenza nucleoprotein and endogenous superantigen. Dev. Immunol. 3, 159-174.
33. McWilliam, A. S., Nelson, D., Thomas, J. A., and Holt, P. G. (1994). Rapid dendritic cell recruitment is a hallmark of the acute inflammatory response at mucosal surfaces. J. Exp. Med. 179, 1331-1336.
34. Mitchell, K. A., and Lawrence, B. P. (2003). Exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) renders influenza virus-specific CD8+ T cells hyporesponsive to antigen. Toxicol. Sci. 74, 74-84.
35. Moskophidis, D., and Kioussis, D. (1998). Contribution of virus-specific CD8+ cytotoxic T cells to virus clearance or pathologic manifestations of influenza virus infection in a T cell receptor transgenic mouse model. J. Exp. Med. 188, 223-232.
36. Neff-LaFord, H., Teske, S., Bushnell, T. P., and Lawrence, B. P. (2007). Aryl hydrocarbon receptor activation during influenza virus infection unveils a novel pathway of IFN-gamma production by phagocytic cells. J. Immunol. 179, 247-255.
37. Nguyen, L. P., and Bradfield, C. A. (2008). The search for endogenous activators of the aryl hydrocarbon receptor. Chem. Res. Toxicol. 21, 102-116.
38. Price, G. E., Ou, R., Jiang, H., Huang, L., and Moskophidis, D. (2000). Viral escape by selection of cytotoxic T cell-resistant variants in influenza A virus pneumonia. J. Exp. Med. 191, 1853-1867.
39. Puga, A., Ma, C., and Marlowe, J. L. (2009). The aryl hydrocarbon receptor cross-talks with multiple signal transduction pathways. Biochem. Pharmacol. 77, 713-722.
40. Ruby, C. E., Funatake, C. J., and Kerkvliet, N. I. (2005). 2,3,7,8 Tetrachlorodibenzo-p-dioxin (TCDD) directly enhances the maturation and apoptosis of dendritic cells in vitro. J. Immunotoxicol. 1, 159-166.
41. Ruby, C. E., Leid, M., and Kerkvliet, N. I. (2002). 2,3,7,8-Tetrachlorodibenzop-dioxin suppresses tumor necrosis factor-alpha and anti-CD40-induced activation of NF-kappaB/Rel in dendritic cells: p50 homodimer activation is not affected. Mol. Pharmacol. 62, 722-728.
42. Shaulov, A., and Murali-Krishna, K. (2008). CD8 T cell expansion and memory differentiation are facilitated by simultaneous and sustained exposure to antigenic and inflammatory milieu. J. Immunol. 180, 1131-1138.
43. Singh, K. P., Casado, F. L., Opanashuk, L. A., and Gasiewicz, T. A. (2009). The aryl hydrocarbon receptor has a normal function in the regulation of hematopoietic and other stem/progenitor cell populations. Biochem. Pharmacol. 77, 577-587.
44. Singh, N. P., Nagarkatti, M., and Nagarkatti, P. (2008). Primary peripheral T cells become susceptible to 2,3,7,8-tetrachlorodibenzo-p-dioxin-mediated apoptosis in vitro upon activation and in the presence of dendritic cells. Mol. Pharmacol. 73, 1722-1735.
45. Stevens, E. A., Mezrich, J. D., and Bradfield, C. A. (2009). The aryl hydrocarbon receptor: a perspective on potential roles in the immune system. Immunology 127, 299-311.
46. Subudhi, S. K., Alegre, M. L., and Fu, Y. X. (2005). The balance of immune responses: costimulation verse coinhibition. J. Mol. Med. 83, 193-202.
47. Teske, S., Bohn, A. A., Regal, J. F., Neumiller, J. J., and Lawrence, B. P. (2005). Activation of the aryl hydrocarbon receptor increases pulmonary neutrophilia and diminishes host resistance to influenza A virus. Am. J. Physiol. Lung Cell. Mol. Physiol. 289, L111-L124.
48. Ueno, H., Klechevsky, E., Morita, R., Aspord, C., Cao, T., Matsui, T., Di Pucchio, T., Connolly, J., Fay, J. W., Pascual, V., et al. (2007). Dendritic cell subsets in health and disease. Immunol. Rev. 219, 118-142.
49. Usherwood, E. J., Hogg, T. L., and Woodland, D. L. (1999). Enumeration of antigen-presenting cells in mice infected with Sendai virus. J. Immunol. 162, 3350-3355.
50. Vermaelen, K. Y., Carro-Muino, I., Lambrecht, B. N., and Pauwels, R. A. (2001). Specific migratory dendritic cells rapidly transport antigen from the airways to the thoracic lymph nodes. J. Exp. Med. 193, 51-60.
51. Vorderstrasse, B. A., Dearstyne, E. A., and Kerkvliet, N. I. (2003). Influence of 2,3,7,8-tetrachlorodibenzo-p-dioxin on the antigen-presenting activity of dendritic cells. Toxicol. Sci. 72, 103-112.
52. Vorderstrasse, B. A., and Kerkvliet, N. I. (2001). 2,3,7,8-Tetrachlorodibenzo-pdioxin affects the number and function of murine splenic dendritic cells and their expression of accessory molecules. Toxicol. Appl. Pharmacol. 171, 117-125.
53. Wack, A., Corbella, P., Harker, N., Crispe, I. N., and Kioussis, D. (1997). Multiple sites of post-activation CD8+ T cell disposal. Eur. J. Immunol. 27, 577-583.
54. Wareing, M. D., Lyon, A. B., Lu, B., Gerard, C., and Sarawar, S. R. (2004). Chemokine expression during the development and resolution of a pulmonary leukocyte response to influenza A virus infection in mice. J. Leukoc. Biol. 76, 886-895.
55. Warren, T. K., Mitchell, K. A., and Lawrence, B. P. (2000). Exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) suppresses the humoral and cell-mediated immune responses to influenza A virus without affecting cytolytic activity in the lung. Toxicol. Sci. 56, 114-123.
56. Weisglas-Kuperus, N., Vreugdenhil, H. J., and Mulder, P. G. (2004). Immunological effects of environmental exposure to polychlorinated biphenyls and dioxins in Dutch school children. Toxicol. Lett. 149, 281-285.
57. Woodland, D. L., Hogan, R. J., and Zhong, W. (2001). Cellular immunity and memory to respiratory virus infections. Immunol. Res. 24, 53-67.
58. Xia, W., Pinto, C. E., and Kradin, R. L. (1995). The antigen-presenting activities of Ia+ dendritic cells shift dynamically from lung to lymph node after an airway challenge with soluble antigen. J. Exp. Med. 181, 1275-1283.
59. Yu, M. L., Hsin, J. W., Hsu, C. C., Chan, W. C., and Guo, Y. L. (1998). The immunologic evaluation of the Yucheng children. Chemosphere 37, 1855-1865.
60. Zheng, P., and Liu, Y. (1997). Costimulation by B7 modulates specificity of cytotoxic T lymphocytes: a missing link that explains some bystander T cell activation. J. Exp. Med. 186, 1787-1791.