The aryl hydrocarbon receptor is a modulator of anti-viral immunity

Biochemical Pharmacology

Volumn 77, Issue 4, 2009, Pages 642-653

  Head, Jennifer L ^a   Lawrence, B Paige ^a  

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

Author keywords

Immune response; Influenza virus; Lung; Neutrophils; T cells

Indexed keywords

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

ADAPTIVE IMMUNITY; CD8+ T LYMPHOCYTE; ENVIRONMENTAL FACTOR; HOST RESISTANCE; HUMAN; IMMUNOMODULATION; IMMUNOTOXICITY; INFLUENZA VIRUS A; INNATE IMMUNITY; INTERFERON PRODUCTION; LEUKOCYTE ACTIVATION; LUNG INFECTION; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; VIRUS INFECTION; VIRUS LATENCY; VIRUS RESISTANCE;

ENVIRONMENTAL POLLUTANTS; HUMANS; IMMUNITY, INNATE; IMMUNOLOGIC FACTORS; INFLUENZA, HUMAN; RECEPTORS, ARYL HYDROCARBON; TETRACHLORODIBENZODIOXIN; VIRUS DISEASES;

EID: 59149105247     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2008.10.031     Document Type: Review

References (118)

1. World Health Organization. Acute Respiratory Infections, 2005. www.who.int/vaccine_research/diseases/ari/en.
2. Anderson R., and Smith B. Deaths: leading causes for 2002. Natl Vital Stat Rep 53 (2005) 1-89
3. Hill A.V. The immunogenetics of human infectious diseases. Annu Rev Immunol 16 (1998) 593-617
4. Colosio C., Birindelli S., Corsini E., Galli C.L., and Maroni M. Low level exposure to chemicals and immune system. Toxicol Appl Pharmacol 207 (2005) 320-328
5. Frampton M.W., Samet J.M., and Utell M.J. Environmental factors and atmospheric pollutants. Semin Respir Infect 6 (1991) 185-193
6. Singh V. The burden of pneumonia in children: an Asian perspective. Paediatr Respir Rev 6 (2005) 88-93
7. Spannhake E.W., Reddy S.P., Jacoby D.B., Yu X.Y., Saatian B., and Tian J. Synergism between rhinovirus infection and oxidant pollutant exposure enhances airway epithelial cell cytokine production. Environ Health Perspect 110 (2002) 665-670
8. Van Den Heuvel R.L., Koppen G., Staessen J.A., Hond E.D., Verheyen G., Nawrot T.S., et al. Immunologic biomarkers in relation to exposure markers of PCBs and dioxins in Flemish adolescents (Belgium). Environ Health Perspect 110 (2002) 595-600
9. Jung D., Berg P.A., Edler L., Ehrenthal W., Fenner D., Flesch-Janys D., et al. Immunologic findings in workers formerly exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin and its congeners. Environ Health Perspect 106 Suppl. 2 (1998) 689-695
10. Tonn T., Esser C., Schneider E.M., Steinmann-Steiner-Haldenstatt W., and Gleichmann E. Persistence of decreased T-helper cell function in industrial workers 20 years after exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Environ Health Perspect 104 (1996) 422-426
11. Weisglas-Kuperus N., Patandin S., Berbers G.A., Sas T.C., Mulder P.G., Sauer P.J., et al. Immunologic effects of background exposure to polychlorinated biphenyls and dioxins in Dutch preschool children. Environ Health Perspect 108 (2000) 1203-1207
12. Sopori M., Goud N., and Kaplan A. Effects of tobacco smoke on the immune systems. In: Dean J., Luster M., and Munson A.I.K. (Eds). Immunotoxicology and Immunopharmacology (1994), Raven Press, New York 413-434
13. Clark D.A., Sweeney G., Safe S., Hancock E., Kilburn D.G., and Gauldie J. Cellular and genetic basis for suppression of cytotoxic T cell generation by haloaromatic hydrocarbons. Immunopharmacology 6 (1983) 143-153
14. Funseth E., Wesslen L., Lindh U., Friman G., and Ilback N.G. Effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on trace elements, inflammation and viral clearance in the myocardium during coxsackievirus B3 infection in mice. Sci Total Environ 284 (2002) 135-147
15. Vorderstrasse B.A., Bohn A.A., and Lawrence B.P. Examining the relationship between impaired host resistance and altered immune function in mice treated with TCDD. Toxicology 188 (2003) 15-28
16. Warren T.K., Mitchell K.A., and Lawrence B.P. 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 (2000) 114-123
17. Burleson G.R., Lebrec H., Yang Y.G., Ibanes J.D., Pennington K.N., and Birnbaum L.S. Effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on influenza virus host resistance in mice. Fundam Appl Toxicol 29 (1996) 40-47
18. Luebke R.W., Copeland C.B., Bishop L.R., Daniels M.J., and Gilmour M.I. Mortality in dioxin-exposed mice infected with influenza: mitochondrial toxicity (reye's-like syndrome) versus enhanced inflammation as the mode of action. Toxicol Sci 69 (2002) 109-116
19. Nohara K., Izumi H., Tamura S., Nagata R., and Tohyama C. Effect of low-dose 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on influenza A virus-induced mortality in mice. Toxicology 170 (2002) 131-138
20. Dempsey P.W., Vaidya S.A., and Cheng G. The art of war: innate and adaptive immune responses. Cell Mol Life Sci 60 (2003) 2604-2621
21. Bender A., Albert M., Reddy A., Feldman M., Sauter B., Kaplan G., et al. The distinctive features of influenza virus infection of dendritic cells. Immunobiology 198 (1998) 552-567
22. Brimnes M.K., Bonifaz L., Steinman R.M., and Moran T.M. Influenza virus-induced dendritic cell maturation is associated with the induction of strong T cell immunity to a coadministered, normally nonimmunogenic protein. J Exp Med 198 (2003) 133-144
23. Legge K.L., and Braciale T.J. Accelerated migration of respiratory dendritic cells to the regional lymph nodes is limited to the early phase of pulmonary infection. Immunity 18 (2003) 265-277
24. Wareing M.D., Lyon A.B., Lu B., Gerard C., and Sarawar S.R. Chemokine expression during the development and resolution of a pulmonary leukocyte response to influenza A virus infection in mice. J Leukoc Biol 76 (2004) 886-895
25. Woodland D.L., Hogan R.J., and Zhong W. Cellular immunity and memory to respiratory virus infections. Immunol Res 24 (2001) 53-67
26. Lawrence B.P., Roberts A.D., Neumiller J.J., Cundiff J.A., and Woodland D.L. Aryl hydrocarbon receptor activation impairs the priming but not the recall of influenza virus-specific CD8+ T cells in the lung. J Immunol 177 (2005) 5819-5828
27. Gerhard W., Mozdzanowska K., Furchner M., Washko G., and Maiese K. Role of the B-cell response in recovery of mice from primary influenza virus infection. Immunol Rev 159 (1997) 95-103
28. Janssen E.M., Lemmens E.E., Wolfe T., Christen U., von Herrath M.G., and Schoenberger S.P. CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 421 (2003) 852-856
29. Hikono H., Kohlmeier J.E., Ely K.H., Scott I., Roberts A.D., Blackman M.A., et al. T-cell memory and recall responses to respiratory virus infections. Immunol Rev 211 (2006) 119-132
30. Doherty P.C., Topham D.J., Tripp R.A., Cardin R.D., Brooks J.W., Stevenson P.G., et al. CD8+ T-cell mechanisms in the control of respiratory virus infections. Immunol Rev 159 (1997) 105-117
31. Kerkvliet N.I. Recent advances in understanding the mechanisms of TCDD immunotoxicity. Int Immunopharmacol 2 (2002) 277-291
32. Lawrence B.P., and Kerkvliet N.I. Immune modulation by TCDD and related polyhalogenated aromatic hydrocarbons. In: Luebke R., House R., and Kimber I. (Eds). Immunotoxicology and Immunopharmacology (2006), CRC Press 239-258
33. Teske S., Bohn A.A., Regal J.F., Neumiller J.J., and Lawrence B.P. Exploring mechanisms that underlie aryl hydrocarbon receptor-mediated increases in pulmonary neutrophilia and diminished host resistance to influenza A virus. Am J Physiol Lung Cell Mol Physiol 289 (2005) 111-124
34. Vorderstrasse B.A., Steppan L.B., Silverstone A.E., and Kerkvliet N.I. Aryl hydrocarbon receptor-deficient mice generate normal immune responses to model antigens and are resistant to TCDD-induced immune suppression. Toxicol Appl Pharmacol 171 (2001) 157-164
35. Nguyen L., and Bradfield C. The search for endogenous activators of the aryl hydrocarbon receptor. Chem Res Toxicol 21 (2008) 102-116
36. White K., Kawabata T., and Ladics G. Mechanisms of polycyclic aromatic hydrocarbon immunotoxicity. In: Dean J., Luster M., Munson A., and Kimber I. (Eds). Immunotoxicology and Immunopharmacology (2005), Raven Press, New York 123-142
37. Martey C.A., Baglole C.J., Gasiewicz T.A., Sime P.J., and Phipps R.P. The aryl hydrocarbon receptor is a regulator of cigarette smoke induction of the cyclooxygenase and prostaglandin pathways in human lung fibroblasts. Am J Physiol Lung Cell Mol Physiol 289 (2005) L391-L399
38. Rodriguez-Sosa M., Elizondo G., Lopez-Duran R.M., Rivera I., Gonzalez F.J., and Vega L. Over-production of IFN-gamma and IL-12 in AhR-null mice. FEBS Lett 579 (2005) 6403-6410
39. Thurmond T.S., Staples J.E., Silverstone A.E., and Gasiewicz T.A. The aryl hydrocarbon receptor has a role in the in vivo maturation of murine bone marrow B lymphocytes and their response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Appl Pharmacol 165 (2000) 227-236
40. House R.V., Lauer L.D., Murray M.J., Thomas P.T., Ehrlich J.P., Burleson G.R., et al. Examination of immune parameters and host resistance mechanisms in B6C3F1 mice following adult exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. J Toxicol Environ Health 31 (1990) 203-215
41. Lawrence B.P., Warren T.K., and Luong H. Fewer T lymphocytes and decreased pulmonary influenza virus burden in mice exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). J Toxicol Environ Health A 61 (2000) 39-53
42. Neff-LaFord H.D., Vorderstrasse B.A., and Lawrence B.P. Fewer CTL, not enhanced NK cells, are sufficient for viral clearance from the lungs of immunocompromised mice. Cell Immunol 226 (2003) 54-64
43. Tate M.D., Brooks A.G., and Reading P.C. The role of neutrophils in the upper and lower respiratory tract during influenza virus infection of mice. Respir Res 9 (2008) 57
44. Fujisawa H. Neutrophils play an essential role in cooperation with antibody in both protection against and recovery from pulmonary infection with influenza virus in mice. J Virol 82 (2008) 2772-2783
45. Smith P., Wang S., Dowling K., and Forsyth K. Leucocyte populations in respiratory syncytial virus-induced bronchiolitis. J Paediatr Child Health 37 (2001) 146-151
46. Tumpey T.M., Garcia-Sastre A., Taubenberger J.K., Palese P., Swayne D.E., Pantin-Jackwood M.J., et al. Pathogenicity of influenza viruses with genes from the 1918 pandemic virus: functional roles of alveolar macrophages and neutrophils in limiting virus replication and mortality in mice. J Virol 79 (2005) 14933-14944
47. Everard M.L., Swarbrick A., Wrightham M., McIntyre J., Dunkley C., James P.D., et al. Analysis of cells obtained by bronchial lavage of infants with respiratory syncytial virus infection. Arch Dis Child 71 (1994) 428-432
48. Yan X.-T., Tumpey T.M., Kunkel S.L., Oakes J.E., and Lausch R.N. Role of MIP-2 in neutrophil migration and tissue injury in Herpes Simplex Virus-1 infected cornea. Invest Ophthalmol Vis Sci 39 (1998) 1854-1862
49. Craigen J.L., Yong K.L., Jordan N.J., Maccormac L.P., Westwick J., Akbar A.N., et al. Human cytomegalovirus infection up-regulates interleukin-8 gene expression and stimulates neutrophil transendothelial migration. Immunology 92 (1997) 138-145
50. Gualano R.C., Hansen M.J., Vlahos R., Jones J.E., Park-Jones R.A., Deliyannis G., et al. Cigarette smoke worsens lung inflammation and impairs resolution of influenza infection in mice. Respir Res 9 (2008) 53
51. Choi J.Y., Oughton J.A., and Kerkvliet N.I. Functional alterations in CD11b(+)Gr-1(+) cells in mice injected with allogeneic tumor cells and treated with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Int Immunopharmacol 3 (2003) 553-570
52. Fan F., Yan B., Wood G., Viluksela M., Rozman K.K., and Cytokines. (IL-1beta and TNFalpha) in relation to biochemical and immunological effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in rats. Toxicology 116 (1997) 9-16
53. Moos A.B., Oughton J.A., and Kerkvliet N.I. The effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on tumor necrosis factor (TNF) production by peritoneal cells. Toxicol Lett 90 (1997) 145-153
54. Vorderstrasse B.A., and Lawrence B.P. Protection against lethal challenge with Streptococcus pneumoniae is conferred by aryl hydrocarbon receptor activation but is not associated with an enhanced inflammatory response. Infect Immun 74 (2006) 5679-5686
55. Kanneganti T.D., Lamkanfi M., and Nunez G. Intracellular NOD-like receptors in host defense and disease. Immunity 27 (2007) 549-559
56. Teske S., Bohn A.A., Hogaboam J.P., and Lawrence B.P. Aryl hydrocarbon receptor targets pathways extrinsic to bone marrow cells to enhance neutrophil recruitment during influenza virus infection. Toxicol Sci 102 (2008) 89-99
57. Bohn A.A., Harrod K.S., Teske S., and Lawrence B.P. Increased mortality associated with TCDD exposure in mice infected with influenza A virus is not due to severity of lung injury or alterations in Clara cell protein content. Chem Biol Interact 155 (2005) 181-190
58. Neff-LaFord H., Teske S., Bushnell T.P., and Lawrence B.P. Aryl hydrocarbon receptor activation during influenza virus infection unveils a novel pathway of IFN-gamma production by phagocytic cells. J Immunol 179 (2007) 247-255
59. Akaike T., and Maeda H. Nitric oxide and virus infection. Immunology 101 (2000) 300-308
60. Karupiah G., Chen J.H., Mahalingam S., Nathan C.F., and MacMicking J.D. Rapid interferon gamma-dependent clearance of influenza A virus and protection from consolidating pneumonitis in nitric oxide synthase 2-deficient mice. J Exp Med 188 (1998) 1541-1546
61. Stark J.M., Khan A.M., Chiappetta C.L., Xue H., Alcorn J.L., Colasurdo G.N., et al. Immune and functional role of nitric oxide in a mouse model of respiratory syncytial virus infection. J Infect Dis 191 (2005) 387-395
62. Fujii S., Akaike T., and Maeda H. Role of nitric oxide in pathogenesis of Herpes Simplex Virus encephalitis in rats. Virology 256 (1999) 203-212
63. Kleinert H., Pautz A., Linker K., and Schwarz P.M. Regulation of the expression of inducible nitric oxide synthase. Eur J Pharmacol 500 (2004) 255-266
64. Mitchell K.A., and Lawrence B.P. Exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) renders influenza virus-specific CD8+ T cells hyporesponsive to antigen. Toxicol Sci 74 (2003) 74-84
65. Mitchell K.A., and Lawrence B.P. T cell receptor transgenic mice provide novel insights into understanding cellular targets of TCDD: suppression of antibody production, but not the response of CD8(+) T cells, during infection with influenza virus. Toxicol Appl Pharmacol 192 (2003) 275-286
66. Maletic N., and Graham B. Cytokine release and innate immunity in respiratory viral infection. Semin Virol 7 (1996) 255-264
67. Guidotti L.G., and Chisari F.V. Noncytolytic control of viral infections by the innate and adaptive immune response. Annu Rev Immunol 19 (2001) 65-91
68. Kerkvliet N.I. AHR-mediated immunomodulation: The role of altered gene transcription. Biochem Pharmacol 77 (2009) 746-760
69. Allan W., Tabi Z., Cleary A., and Doherty P.C. Cellular events in the lymph node and lung of mice with influenza. Consequences of depleting CD4+ T cells. J Immunol 144 (1990) 3980-3986
70. Chen W., Bennink J.R., Morton P.A., and Yewdell J.W. Mice deficient in perforin, CD4+ T cells, or CD28-mediated signaling maintain the typical immunodominance hierarchies of CD8+ T-cell responses to influenza virus. J Virol 76 (2002) 10332-10337
71. Belz G.T., Wodarz D., Diaz G., Nowak M.A., and Doherty P.C. Compromised influenza virus-specific CD8(+)-T-cell memory in CD4(+)-T-cell-deficient mice. J Virol 76 (2002) 12388-12393
72. Lawrence B.P., and Vorderstrasse B.A. Activation of the aryl hydrocarbon receptor diminishes the memory response to homotypic influenza virus infection but does not impair host resistance. Toxicol Sci 79 (2004) 304-314
73. Kerkvliet N.I., and Brauner J.A. Mechanisms of 1,2,3,4,6,7,8-heptachlorodibenzo-p-dioxin (HpCDD)-induced humoral immune suppression: evidence of primary defect in T-cell regulation. Toxicol Appl Pharmacol 87 (1987) 18-31
74. Sulentic C.E., Holsapple M.P., and Kaminski N.E. Aryl hydrocarbon receptor-dependent suppression by 2,3,7,8-tetrachlorodibenzo-p-dioxin of IgM secretion in activated B cells. Mol Pharmacol 53 (1998) 623-629
75. Wood S.C., and Holsapple M.P. Direct suppression of superantigen-induced IgM secretion in human lymphocytes by 2,3,7,8-TCDD. Toxicol Appl Pharmacol 122 (1993) 308-313
76. Shepherd D.M., Dearstyne E.A., and Kerkvliet N.I. The effects of TCDD on the activation of ovalbumin (OVA)-specific DO11.10 transgenic CD4(+) T cells in adoptively transferred mice. Toxicol Sci 56 (2000) 340-350
77. Moran R.A., Lee C.W., Fujimoto J.M., and Calvanico N.J. Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on IgA serum and bile levels in rats. Immunopharmacology 12 (1986) 245-250
78. Tecle T., White M.R., Gantz D., Crouch E.C., and Hartshorn K.L. Human neutrophil defensins increase neutrophil uptake of influenza A virus and bacteria and modify virus-induced respiratory burst responses. J Immunol 178 (2007) 8046-8052
79. Ueno H., Klechevsky E., Morita R., Aspord C., Cao T., Matsui T., et al. Dendritic cell subsets in health and disease. Immunol Rev 219 (2007) 118-142
80. Vorderstrasse B.A., Dearstyne E.A., and Kerkvliet N.I. Influence of 2,3,7,8-tetrachlorodibenzo-p-dioxin on the antigen-presenting activity of dendritic cells. Toxicol Sci 72 (2003) 103-112
81. Vorderstrasse B.A., and Kerkvliet N.I. 2,3,7,8-Tetrachlorodibenzo-p-dioxin affects the number and function of murine splenic dendritic cells and their expression of accessory molecules. Toxicol Appl Pharmacol 171 (2001) 117-125
82. Laupeze B., Amiot L., Sparfel L., Le Ferrec E., Fauchet R., and Fardel O. Polycyclic aromatic hydrocarbons affect functional differentiation and maturation of human monocyte-derived dendritic cells. J Immunol 168 (2002) 2652-2658
83. Ruby C.E., Funatake C.J., and Kerkvliet N.I. 2,3,7,8 Tetrachlorodibenzo-p-dioxin (TCDD) directly enhances the maturation and apoptosis of dendritic cells in vitro. J Immunotoxicol 1 (2004) 159-166
84. Ruby C.E., Leid M., and Kerkvliet N.I. 2,3,7,8-Tetrachlorodibenzo-p-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 (2002) 722-728
85. Lawrence B.P., Denison M.S., Novak H., Vorderstrasse B.A., Harrer N., Neruda W., et al. Activation of the aryl hydrocarbon receptor is essential for mediating the anti-inflammatory effects of a novel low molecular weight compound. Blood (2008)
86. Lee J.A., Hwang J.A., Sung H.N., Jeon C.H., Gill B.C., Youn H.J., et al. 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 (2007) 31-40
87. Funatake C.J., Marshall N.B., Steppan L.B., Mourich D.V., and Kerkvliet N.I. Cutting edge: activation of the aryl hydrocarbon receptor by 2,3,7,8-tetrachlorodibenzo-p-dioxin generates a population of CD4+ CD25+ cells with characteristics of regulatory T cells. J Immunol 175 (2005) 4184-4188
88. Kimura A., Naka T., Nohara K., Fujii-Kuriyama Y., and Kishimoto T. Aryl hydrocarbon receptor regulates Stat1 activation and participates in the development of Th17 cells. Proc Natl Acad Sci USA 105 (2008) 9721-9726
89. Veldhoen M., Hirota K., Westendorf A.M., Buer J., Dumoutier L., Renauld J.C., et al. The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 453 (2008) 106-109
90. Quintana F.J., Basso A.S., Iglesias A.H., Korn T., Farez M.F., Bettelli E., et al. Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature 453 (2008) 65-71
91. Haeryfar S.M., DiPaolo R.J., Tscharke D.C., Bennink J.R., Yewdell J.W., and Regulatory. T cells suppress CD8+ T cell responses induced by direct priming and cross-priming and moderate immunodominance disparities. J Immunol 174 (2005) 3344-3351
92. Belkaid Y., and Rouse B.T. Natural regulatory T cells in infectious disease. Nat Immunol 6 (2005) 353-360
93. Zhou Y. Regulatory T cells and viral infections. Front Biosci 13 (2008) 1152-1170
94. Zhang N., and Walker M.K. Crosstalk between the aryl hydrocarbon receptor and hypoxia on the constitutive expression of cytochrome P4501A1 mRNA. Cardiovasc Toxicol 7 (2007) 282-290
95. Chang H., Chang L.W., Cheng Y.H., Tsai W.T., Tsai M.X., and Lin P. Preferential induction of CYP1A1 and CYP1B1 in CCSP-positive cells. Toxicol Sci 89 (2006) 205-213
96. Lang D.S., Becker S., Devlin R.B., and Koren H.S. Cell-specific differences in the susceptibility of potential cellular targets of human origin derived from blood and lung following treatment with 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Cell Biol Toxicol 14 (1998) 23-38
97. Kashuba E., Kashuba V., Pokrovskaja K., Klein G., and Szekely L. Epstein-Barr virus encoded nuclear protein EBNA-3 binds XAP-2, a protein associated with Hepatitis B virus X antigen. Oncogene 19 (2000) 1801-1806
98. Kashuba E.V., Gradin K., Isaguliants M., Szekely L., Poellinger L., Klein G., et al. Regulation of transactivation function of the aryl hydrocarbon receptor by the Epstein-Barr virus-encoded EBNA-3 protein. J Biol Chem 281 (2006) 1215-1223
99. Kuppers R. B cells under influence: transformation of B cells by Epstein-Barr virus. Nat Rev Immunol 3 (2003) 801-812
100. Hardell L., Lindstrom G., van Bavel B., Hardell K., Linde A., Carlberg M., et al. Adipose tissue concentrations of dioxins and dibenzofurans, titers of antibodies to Epstein-Barr virus early antigen and the risk for non-Hodgkin lymphoma. Environ Res 87 (2001) 99-107
101. Stancek D., Kosecka G., Oltman M., Keleova A., and Jahnova E. Links between prolonged exposure to xenobiotics, increased incidence of hepatopathies, immunological disturbances and exacerbation of latent Epstein-Barr virus infections. Int J Immunopharmacol 17 (1995) 321-328
102. Yao Y., Hoffer A., Chang C.Y., and Puga A. Dioxin activates HIV-1 gene expression by an oxidative stress pathway requiring a functional cytochrome P450 CYP1A1 enzyme. Environ Health Perspect 103 (1995) 366-371
103. Gollapudi S., Kim C.H., Patel A., Sindhu R., and Gupta S. Dioxin activates human immunodeficiency virus-1 expression in chronically infected promonocytic U1 cells by enhancing NF-kappa B activity and production of tumor necrosis factor-alpha. Biochem Biophys Res Commun 226 (1996) 889-894
104. Ohata H., Tetsuka T., Hayashi H., Onozaki K., and Okamoto T. 3-Methylcholanthrene activates human immunodeficiency virus type 1 replication via aryl hydrocarbon receptor. Microbiol Immunol 47 (2003) 363-370
105. Tsyrlov I.B., and Pokrovsky A. Stimulatory effect of the CYP1A1 inducer 2,3,7,8-tetrachlorodibenzo-p-dioxin on the reproduction of HIV-1 in human lymphoid cell culture. Xenobiotica 23 (1993) 457-467
106. Murayama T., Inoue M., Nomura T., Mori S., and Eizuru Y. 2,3,7,8-Tetrachlorodibenzo-p-dioxin is a possible activator of human cytomegalovirus replication in a human fibroblast cell line. Biochem Biophys Res Commun 296 (2002) 651-656
107. Denison M.S., and Nagy S.R. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu Rev Pharmacol Toxicol 43 (2003) 309-334
108. Fujii-Kuriyama Y., and Mimura J. Molecular mechanisms of AhR functions in the regulation of cytochrome P450 genes. Biochem Biophys Res Commun 338 (2005) 311-317
109. Carver L.A., and Bradfield C.A. Ligand-dependent interaction of the aryl hydrocarbon receptor with a novel immunophilin homolog in vivo. J Biol Chem 272 (1997) 11452-11456
110. Kim D.W., Gazourian L., Quadri S.A., Romieu-Mourez R., Sherr D.H., and Sonenshein G.E. The RelA NF-kappaB subunit and the aryl hydrocarbon receptor (AhR) cooperate to transactivate the c-myc promoter in mammary cells. Oncogene 19 (2000) 5498-5506
111. Meyer B.K., Pray-Grant M.G., Vanden Heuvel J.P., and Perdew G.H. Hepatitis B virus X-associated protein 2 is a subunit of the unliganded aryl hydrocarbon receptor core complex and exhibits transcriptional enhancer activity. Mol Cell Biol 18 (1998) 978-988
112. Tian Y., Ke S., Denison M.S., Rabson A.B., and Gallo M.A. Ah receptor and NF-kappaB interactions, a potential mechanism for dioxin toxicity. J Biol Chem 274 (1999) 510-515
113. Puga A., Barnes S.J., Chang C., Zhu H., Nephew K.P., Khan S.A., et al. Activation of transcription factors activator protein-1 and nuclear factor-kappaB by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Biochem Pharmacol 59 (2000) 997-1005
114. Puga A., Barnes S.J., Dalton T.P., Chang C., Knudsen E.S., and Maier M.A. Aromatic hydrocarbon receptor interaction with the retinoblastoma protein potentiates repression of E2F-dependent transcription and cell cycle arrest. J Biol Chem 275 (2000) 2943-2950
115. Lai Z.W., Pineau T., and Esser C. Identification of dioxin-responsive elements (DREs) in the 5′ regions of putative dioxin-inducible genes. Chem Biol Interact 100 (1996) 97-112
116. Zeytun A., McKallip R.J., Fisher M., Camacho I., Nagarkatti M., and Nagarkatti P.S. Analysis of 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced gene expression profile in vivo using pathway-specific cDNA arrays. Toxicology 178 (2002) 241-260
117. Boverhof D.R., Tam E., Harney A.S., Crawford R.B., Kaminski N.E., and Zacharewski T.R. 2,3,7,8-Tetrachlorodibenzo-p-dioxin induces suppressor of cytokine signaling 2 in murine B cells. Mol Pharmacol 66 (2004) 1662-1670
118. Nagai H., Takei T., Tohyama C., Kubo M., Abe R., and Nohara K. Search for the target genes involved in the suppression of antibody production by TCDD in C57BL/6 mice. Int Immunopharmacol 5 (2005) 331-343