Effects of developmental activation of the AhR on CD4+ T-cell responses to influenza virus infection in adult mice

Environmental Health Perspectives

Volumn 122, Issue 11, 2014, Pages 1201-1208

  Boule, Lisbeth A ^a   Winans, Bethany ^b   Paige Lawrence, B ^a,b  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2, 3, 7, 8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; UNCLASSIFIED DRUG; 2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN;

ADOPTIVE TRANSFER; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; FLOW CYTOMETRY; INFLUENZA; INFLUENZA VIRUS A; MALE; MOUSE; NONHUMAN; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; AGONISTS; ANIMAL; C57BL MOUSE; DRUG EFFECTS; ENVIRONMENTAL EXPOSURE; IMMUNOLOGY; INFLUENZA A VIRUS; LYMPHOCYTE ACTIVATION; METABOLISM; ORTHOMYXOVIRUS INFECTION;

ANIMALIA; INFLUENZA A VIRUS; MUS; ORTHOMYXOVIRIDAE;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; FEMALE; INFLUENZA A VIRUS; LYMPHOCYTE ACTIVATION; MALE; MATERNAL EXPOSURE; MICE; MICE, INBRED C57BL; ORTHOMYXOVIRIDAE INFECTIONS; RECEPTORS, ARYL HYDROCARBON; TETRACHLORODIBENZODIOXIN;

EID: 84928498198     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1408110     Document Type: Article

References (47)

1. Alam S, Knowlden ZA, Sangster MY, Sant AJ. 2014. CD4 T cell help is limiting and selective during the primary B cell response to influenza virus infection. J Virol 88(1):314–324.
2. Almansa R, Socias L, Ramirez P, Martin-Loeches I, Valles J, Loza A, et al. 2011. Imbalanced pro- and anti-Th17 responses (IL-17/granulocyte colony-stimulating factor) predict fatal outcome in 2009 pandemic influenza. Crit Care 15(5):448; doi:10.1186/cc10426.
3. Boekelheide K, Blumberg B, Chapin RE, Cote I, Graziano JH, Janesick A, et al. 2012. Predicting later-life outcomes of early-life exposures. Environ Health Perspect 120:1353–1361; doi:10.1289/ehp.1204934.
4. Boyden AW, Legge KL, Waldschmidt TJ. 2012. Pulmonary infection with influenza A virus induces site-specific germinal center and T follicular helper cell responses. PLoS One 7(7):e40733; doi:10.1371/journal.pone.0040733.
5. Brand S, Kesper DA, Teich R, Kilic-Niebergall E, Pinkenburg O, Bothur E, et al. 2012. DNA methylation of TH1/TH2 cytokine genes affects sensitization and progress of experimental asthma. J Allergy Clin Immunol 129(6):1602–1610.e1606.
6. Camacho IA, Singh N, Hegde VL, Nagarkatti M, Nagarkatti PS. 2005. Treatment of mice with 2,3,7,8-tetrachlorodibenzop- dioxin leads to aryl hydrocarbon receptor-dependent nuclear translocation of NF-κB and expression of Fas ligand in thymic stromal cells and consequent apoptosis in T cells. J Immunol 175(1):90–103.
7. Cantone I, Fisher AG. 2013. Epigenetic programming and reprogramming during development. Nat Struct Mol Biol 20(3):282–289.
8. Carson WF IV, Cavassani KA, Ito T, Schaller M, Ishii M, Dou Y, et al. 2010. Impaired CD4+ T-cell proliferation and effector function correlates with repressive histone methylation events in a mouse model of severe sepsis. Eur J Immunol 40(4):998–1010.
9. Chapman TJ, Castrucci MR, Padrick RC, Bradley LM, Topham DJ. 2005. Antigen-specific and non-specific CD4+ T cell recruitment and proliferation during influenza infection. Virology 340(2):296–306.
10. Cohen SB, Maurer KJ, Egan CE, Oghumu S, Satoskar AR, Denkers EY. 2013. CXCR3-dependent CD4+ T cells are required to activate inflammatory monocytes for defense against intestinal infection. PLoS Pathog 9(10):e1003706; doi:10.1371/journal.ppat.1003706.
11. Dallaire F, Dewailly E, Vezina C, Muckle G, Weber JP, Bruneau S, et al. 2006. Effect of prenatal exposure to polychlorinated biphenyls on incidence of acute respiratory infections in preschool Inuit children. Environ Health Perspect 114:1301–1305; doi:10.1289/ehp.8683.
12. Dittel BN. 2008. CD4 T cells: balancing the coming and going of autoimmune-mediated inflammation in the CNS. Brain Behav Immun 22(4):421–430; doi:10.1016/j.bbi.2007.11.010.
13. Faith RE, Moore JA. 1977. Impairment of thymus-dependent immune functions by exposure of the developing immune system to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). J Toxicol Environ Health 3(3):451–464.
14. Fontenot JD, Rudensky AY. 2005. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat Immunol 6(4):331–337.
15. Gehrs BC, Smialowicz RJ. 1999. Persistent suppression of delayed-type hypersensitivity in adult F344 rats after perinatal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicology 134(1):79–88.
16. Glynn A, Thuvander A, Aune M, Johannisson A, Darnerud PO, Ronquist G, et al. 2008. Immune cell counts and risks of respiratory infections among infants exposed pre- and postnatally to organochlorine compounds: a prospective study. Environ Health 7:62; doi:10.1186/1476-069X-7-62.
17. Heilmann C, Budtz-Jorgensen E, Nielsen F, Heinzow B, Weihe P, Grandjean P. 2010. Serum concentrations of antibodies against vaccine toxoids in children exposed perinatally to immunotoxicants. Environ Health Perspect 118:1434–1438; doi:10.1289/ehp.1001975.
18. Hochstenbach K, van Leeuwen DM, Gmuender H, Gottschalk RW, Stolevik SB, Nygaard UC, et al. 2012. Toxicogenomic profiles in relation to maternal immunotoxic exposure and immune functionality in newborns. Toxicol Sci 129(2):315–324.
19. Hogaboam JP, Moore AJ, Lawrence BP. 2008. The aryl hydrocarbon receptor affects distinct tissue compartments during ontogeny of the immune system. Toxicol Sci 102(1):160–170.
20. Institute of Medicine. 2003. Dioxins and Dioxin-like Compounds in the Food Supply. Washington, DC:National Academies Press. Available: http://www.nap.edu/openbook. php?record_id=10763 [accessed 7 October 2014].
21. Jensen BA, Leeman RJ, Schlezinger JJ, Sherr DH. 2003. Aryl hydrocarbon receptor (AhR) agonists suppress interleukin-6 expression by bone marrow stromal cells: an immunotoxicology study. Environ Health 2(1):16; doi:10.1186/1476-069X-2-16.
22. Jin GB, Winans B, Martin KC, Lawrence BP. 2014. New insights into the role of the aryl hydrocarbon receptor in the function of CD11c+ cells during respiratory viral infection. Eur J Immunol 44(6):1685–1698; doi:10.1002/eji.201343980.
23. Leveton C, Barnass S, Champion B, Lucas S, De Souza B, Nicol M, et al. 1989. T-cell-mediated protection of mice against virulent Mycobacterium tuberculosis. Infect Immun 57(2):390–395.
24. Luster MI, Boorman GA, Dean JH, Harris MW, Luebke RW, Padarathsingh ML, et al. 1980. Examination of bone marrow, immunologic parameters and host susceptibility following pre- and postnatal exposure to 2,3,7,8-tetrachlorodibenzop- dioxin (TCDD). Int J Immunopharmacol 2(4):301–310.
25. Malley R, Trzcinski K, Srivastava A, Thompson CM, Anderson PW, Lipsitch M. 2005. CD4+ T cells mediate antibody-independent acquired immunity to pneumococcal colonization. Proc Natl Acad Sci USA 102(13):4848–4853.
26. Manikkam M, Tracey R, Guerrero-Bosagna C, Skinner MK. 2012. Dioxin (TCDD) induces epigenetic transgenerational inheritance of adult onset disease and sperm epimutations. PLoS One 7(9):e46249; doi:10.1371/journal.pone.0046249.
27. McKinstry KK, Strutt TM, Buck A, Curtis JD, Dibble JP, Huston G, et al. 2009. IL-10 deficiency unleashes an influenza-specific Th17 response and enhances survival against high-dose challenge. J Immunol 182(12):7353–7363.
28. Mebius RE. 2003. Organogenesis of lymphoid tissues. Nat Rev Immunol 3(4):292–303.
29. Mustafa A, Holladay SD, Witonsky S, Sponenberg DP, Karpuzoglu E, Gogal RM Jr. 2011. A single mid-gestation exposure to TCDD yields a postnatal autoimmune signature, differing by sex, in early geriatric C57BL/6 mice. Toxicology 290(2–3):156–168.
30. Papoutsis AJ, Selmin OI, Borg JL, Romagnolo DF. 2013. Gestational exposure to the AhR agonist 2,3,7,8-tetrachlorodibenzo- p-dioxin induces BRCA-1 promoter hypermethylation and reduces BRCA-1 expression in mammary tissue of rat offspring: preventive effects of resveratrol. Mol Carcinog; doi:10.1002/mc.22095.
31. Quintana FJ, Sherr DH. 2013. Aryl hydrocarbon receptor control of adaptive immunity. Pharmacol Rev 65(4):1148–1161.
32. Schecter A, Cramer P, Boggess K, Stanley J, Papke O, Olson J, et al. 2001. Intake of dioxins and related compounds from food in the U.S. population. J Toxicol Environ Health A 63(1):1–18.
33. Singh NP, Singh UP, Singh B, Price RL, Nagarkatti M, Nagarkatti PS. 2011. Activation of aryl hydrocarbon receptor (AhR) leads to reciprocal epigenetic regulation of FoxP3 and IL-17 expression and amelioration of experimental colitis. PLoS One 6(8):e23522; doi:10.1371/journal.pone.0023522.
34. Smith CM, Wilson NS, Waithman J, Villadangos JA, Carbone FR, Heath WR, et al. 2004. Cognate CD4+ T cell licensing of dendritic cells in CD8+ T cell immunity. Nat Immunol 5(11):1143–1148.
35. Stolevik SB, Nygaard UC, Namork E, Haugen M, Meltzer HM, Alexander J, et al. 2013. Prenatal exposure to polychlorinated biphenyls and dioxins from the maternal diet may be associated with immunosuppressive effects that persist into early childhood. Food Chem Toxicol 51:165–172.
36. Sugita-Konishi Y, Kobayashi K, Naito H, Miura K, Suzuki Y. 2003. Effect of lactational exposure to 2,3,7,8-tetrachlorodibenzo- p-dioxin on the susceptibility to Listeria infection. Biosci Biotechnol Biochem 67(1):89–93.
37. Sulentic CE, Kaminski NE. 2011. The long winding road toward understanding the molecular mechanisms for B-cell suppression by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Sci 120(suppl 1):S171–S191.
38. Teske S, Bohn AA, Regal JF, Neumiller JJ, Lawrence BP. 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(1):L111–L124.
39. Thomas PT, Hinsdill RD. 1979. The effect of perinatal exposure to tetrachlorodibenzo-p-dioxin on the immune response of young mice. Drug Chem Toxicol 2(1–2):77–98.
40. Vock C, Hauber HP, Wegmann M. et al. 2010. The other T helper cells in asthma pathogenesis. J Allergy 2010:519298; doi:10.1155/2010/519298.
41. Vorderstrasse BA, Cundiff JA, Lawrence BP. 2004. Developmental exposure to the potent aryl hydrocarbon receptor agonist 2,3,7,8-tetrachlorodibenzo-p-dioxin impairs the cell-mediated immune response to infection with influenza A virus, but enhances elements of innate immunity. J Immunotoxicol 1(2):103–112.
42. Vorderstrasse BA, Cundiff JA, Lawrence BP. 2006. A doseresponse study of the effects of prenatal and lactational exposure to TCDD on the immune response to influenza A virus. J Toxicol Environ Health A 69(6):445–463.
43. Vos JG, Moore JA. 1974. Suppression of cellular immunity in rats and mice by maternal treatment with 2,3,7,8-tetrachlorodibenzo- p-dioxin. Int Arch Allergy Appl Immunol 47(5):777–794.
44. Warren TK, Mitchell KA, Lawrence BP. 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(1):114–123.
45. Wheeler JL, Martin KC, Lawrence BP. 2013. Novel cellular targets of AhR underlie alterations in neutrophilic inflammation and inducible nitric oxide synthase expression during influenza virus infection. J Immunol 190(2):659–668.
46. Winans B, Humble MC, Lawrence BP. 2011. Environmental toxicants and the developing immune system: a missing link in the global battle against infectious disease? Reprod Toxicol 31(3):327–336.
47. + T cells towards distinct T-helper cell subsets. Immunol Rev 252(1):12–23.