Linking the aryl hydrocarbon receptor with altered DNA methylation patterns and developmentally induced aberrant antiviral CD8+ T cell responses

Journal of Immunology

Volumn 194, Issue 9, 2015, Pages 4446-4457

  Winans, Bethany ^a   Nagari, Anusha ^b   Chae, Minho ^b   Post, Christina M ^a   Ko, Chia I ^c   Puga, Alvaro ^c   Kraus, W Lee ^b   Lawrence, B Paige ^a  

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

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION; HIGH THROUGHPUT SEQUENCING; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOREGULATION; INFLUENZA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RECEPTOR BINDING; T LYMPHOCYTE ACTIVATION; ANIMAL; DISEASE MODEL; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; MALE; METABOLISM; VIRUS INFECTION;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; DNA METHYLATION; FEMALE; GENE EXPRESSION PROFILING; MALE; MICE; MICE, KNOCKOUT; PROMOTER REGIONS, GENETIC; RECEPTORS, ARYL HYDROCARBON; VIRUS DISEASES;

EID: 84928474100     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402044     Document Type: Article

References (73)

1. Dallaire, F., E. Dewailly, C. Vézina, G. Muckle, J. P. Weber, S. Bruneau, and P. Ayotte. 2006. Effect of prenatal exposure to polychlorinated biphenyls on incidence of acute respiratory infections in preschool Inuit children. Environ. Health Perspect. 114: 1301-1305.
2. Heilmann, C., E. Budtz-Jørgensen, F. Nielsen, B. Heinzow, P. Weihe, and P. Grandjean. 2010. Serum concentrations of antibodies against vaccine toxoids in children exposed perinatally to immunotoxicants. Environ. Health Perspect. 118: 1434-1438.
3. Heilmann, C., P. Grandjean, P. Weihe, F. Nielsen, and E. Budtz-Jørgensen. 2006. Reduced antibody responses to vaccinations in children exposed to polychlorinated biphenyls. PLoS Med. 3: e311.
4. Glynn, A., A. Thuvander, M. Aune, A. Johannisson, P. O. Darnerud, G. Ronquist, and S. Cnattingius. 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.
5. Stølevik, S. B., U. C. Nygaard, E. Namork, M. Haugen, H. E. Kvalem, H. M. Meltzer, J. Alexander, J. H. van Delft, Hv. Loveren, M. Løvik, and B. Granum. 2011. Prenatal exposure to polychlorinated biphenyls and dioxins is associated with increased risk of wheeze and infections in infants. Food Chem. Toxicol. 49: 1843-1848.
6. Stølevik, S. B., U. C. Nygaard, E. Namork, M. Haugen, H. M. Meltzer, J. Alexander, H. K. Knutsen, I. Aaberge, K. Vainio, H. van Loveren, 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.
7. Barouki, R., P. D. Gluckman, P. Grandjean, M. Hanson, and J. J. Heindel. 2012. Developmental origins of non-communicable disease: implications for research and public health. Environ. Health 11: 42.
8. Quintana, F. J., and D. H. Sherr. 2013. Aryl hydrocarbon receptor control of adaptive immunity. Pharmacol. Rev. 65: 1148-1161.
9. Nguyen, L. P., and C. A. Bradfield. 2008. The search for endogenous activators of the aryl hydrocarbon receptor. Chem. Res. Toxicol. 21: 102-116.
10. Winans, B., M. C. Humble, and B. P. Lawrence. 2011. Environmental toxicants and the developing immune system: a missing link in the global battle against infectious disease? Reprod. Toxicol. 31: 327-336.
11. Vorderstrasse, B. A., J. A. Cundiff, and B. P. Lawrence. 2004. Developmental exposure to the potent aryl hydrocarbon receptor agonist 2,3,7,8-tetra-chlorodibenzo-p-dioxin impairs the cell-mediated immune response to infection with influenza a virus, but enhances elements of innate immunity. J. Immunotoxicol. 1: 103-112.
12. Hogaboam, J. P., A. J. Moore, and B. P. Lawrence. 2008. The aryl hydrocarbon receptor affects distinct tissue compartments during ontogeny of the immune system. Toxicol. Sci. 102: 160-170.
13. Luebke, R. W., D. H. Chen, R. Dietert, Y. Yang, M. King, and M. I. Luster, Immunotoxicology Workgroup. 2006. The comparative immunotoxicity of five selected compounds following developmental or adult exposure. J. Toxicol. Environ. Health B Crit. Rev. 9: 1-26.
14. Szyf, M., and J. Bick. 2013. DNA methylation: a mechanism for embedding early life experiences in the genome. Child Dev. 84: 49-57.
15. Dolinoy, D. C., J. R. Weidman, and R. L. Jirtle. 2007. Epigenetic gene regulation: linking early developmental environment to adult disease. Reprod. Toxicol. 23: 297-307.
16. Daxinger, L., and E. Whitelaw. 2010. Transgenerational epigenetic inheritance: more questions than answers. Genome Res. 20: 1623-1628.
17. Jirtle, R. L., and M. K. Skinner. 2007. Environmental epigenomics and disease susceptibility. Nat. Rev. Genet. 8: 253-262.
18. Jones, P. A. 2012. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet. 13: 484-492.
19. Suárez-Álvarez, B., A. Baragaño Raneros, F. Ortega, and C. López-Larrea. 2013. Epigenetic modulation of the immune function: a potential target for tolerance. Epigenetics 8: 694-702.
20. Wu, Q., S. Ohsako, R. Ishimura, J. S. Suzuki, and C. Tohyama. 2004. Exposure of mouse preimplantation embryos to 2,3,7,8-tetrachlorodibenzo-p -dioxin (TCDD) alters the methylation status of imprinted genes H19 and Igf2. Biol. Reprod. 70: 1790-1797.
21. Manikkam, M., R. Tracey, C. Guerrero-Bosagna, and M. K. Skinner. 2012. Dioxin (TCDD) induces epigenetic transgenerational inheritance of adult onset disease and sperm epimutations. PLoS ONE 7: e46249.
22. Papoutsis, A. J., O. I. Selmin, J. L. Borg, and D. F. Romagnolo. 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.
23. Somm, E., C. Stouder, and A. Paoloni-Giacobino. 2013. Effect of developmental dioxin exposure on methylation and expression of specific imprinted genes in mice. Reprod. Toxicol. 35: 150-155.
24. Intarasunanont, P., P. Navasumrit, S. Waraprasit, K. Chaisatra, W. A. Suk, C. Mahidol, and M. Ruchirawat. 2012. Effects of arsenic exposure on DNA methylation in cord blood samples from newborn babies and in a human lymphoblast cell line. Environ. Health 11: 31.
25. Kile, M. L., E. A. Houseman, A. A. Baccarelli, Q. Quamruzzaman, M. Rahman, G. Mostofa, A. Cardenas, R. O. Wright, and D. C. Christiani. 2014. Effect of prenatal arsenic exposure on DNA methylation and leukocyte subpopulations in cord blood. Epigenetics 9: 774-782.
26. Koestler, D. C., M. Avissar-Whiting, E. A. Houseman, M. R. Karagas, and C. J. Marsit. 2013. Differential DNA methylation in umbilical cord blood of infants exposed to low levels of arsenic in utero. Environ. Health Perspect. 121: 971-977.
27. Pilsner, J. R., H. Hu, A. Ettinger, B. N. Sánchez, R. O. Wright, D. Cantonwine, A. Lazarus, H. Lamadrid-Figueroa, A. Mercado-Garciá, M. M. Té llez-Rojo, and M. Hernández-Avila. 2009. Influence of prenatal lead exposure on genomic methylation of cord blood DNA. Environ. Health Perspect. 117: 1466-1471.
28. Sanders, A. P., L. Smeester, D. Rojas, T. DeBussycher, M. C. Wu, F. A. Wright, Y. H. Zhou, J. E. Laine, J. E. Rager, G. K. Swamy, et al. 2014. Cadmium exposure and the epigenome: exposure-associated patterns of DNA methylation in leukocytes from mother-baby pairs. Epigenetics 9: 212-221.
29. Joubert, B. R., S. E. Håberg, R. M. Nilsen, X. Wang, S. E. Vollset, S. K. Murphy, Z. Huang, C. Hoyo, Ø. Midttun, L. A. Cupul-Uicab, et al. 2012. 450K epigenome-wide scan identifies differential DNA methylation in newborns related to maternal smoking during pregnancy. Environ. Health Perspect. 120: 1425-1431.
30. Wang, I. J., S. L. Chen, T. P. Lu, E. Y. Chuang, and P. C. Chen. 2013. Prenatal smoke exposure, DNA methylation, and childhood atopic dermatitis. Clin. Exp. Allergy 43: 535-543.
31. Tang, W. Y., L. Levin, G. Talaska, Y. Y. Cheung, J. Herbstman, D. Tang, R. L. Miller, F. Perera, and S. M. Ho. 2012. Maternal exposure to polycyclic aromatic hydrocarbons and 59-CpG methylation of interferon-γ in cord white blood cells. Environ. Health Perspect. 120: 1195-1200.
32. Reinius, L. E., N. Acevedo, M. Joerink, G. Pershagen, S. E. Dahlé n, D. Greco, C. Söderhäll, A. Scheynius, and J. Kere. 2012. Differential DNA methylation in purified human blood cells: implications for cell lineage and studies on disease susceptibility. PLoS ONE 7: e41361.
33. Kohlmeier, J. E., and D. L. Woodland. 2009. Immunity to respiratory viruses. Annu. Rev. Immunol. 27: 61-82.
34. Scharer, C. D., B. G. Barwick, B. A. Youngblood, R. Ahmed, and J. M. Boss. 2013. Global DNA methylation remodeling accompanies CD8 T cell effector function. J. Immunol. 191: 3419-3429.
35. Boule, L. A., B. Winans, and B. P. Lawrence. 2014. Effects of developmental activation of the AhR on CD4 T-cell responses to influenza virus infection in adult mice. Environ. Health Perspect. 122: 1201-1208.
36. Down, T. A., V. K. Rakyan, D. J. Turner, P. Flicek, H. Li, E. Kulesha, S. Gräf, N. Johnson, J. Herrero, E. M. Tomazou, et al. 2008. A Bayesian deconvolution strategy for immunoprecipitation-based DNA methylome analysis. Nat. Biotechnol. 26: 779-785.
37. Ko, C. I., Q. Wang, Y. Fan, Y. Xia, and A. Puga. 2014. Pluripotency factors and polycomb group proteins repress aryl hydrocarbon receptor expression in murine embryonic stem cells. Stem Cell Res. (Amst.) 12: 296-308.
38. + cells during respiratory viral infection. Eur. J. Immunol. 44: 1685-1698.
39. Attwood, J., and B. Richardson. 2004. Relative quantitation of DNA methyltransferase mRNA by real-time RT-PCR assay. Methods Mol. Biol. 287: 273-283.
40. Phillips, J. M., L. D. Burgoon, and J. I. Goodman. 2009. The constitutive active/androstane receptor facilitates unique phenobarbital-induced expression changes of genes involved in key pathways in precancerous liver and liver tumors. Toxicol. Sci. 110: 319-333.
41. Wheeler, J. L., K. C. Martin, E. Resseguie, and B. P. Lawrence. 2014. Differential consequences of two distinct AhR ligands on innate and adaptive immune responses to influenza A virus. Toxicol. Sci. 137: 324-334.
42. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 22DDC(T) method. Methods 25: 402-408.
43. Langmead, B., C. Trapnell, M. Pop, and S. L. Salzberg. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10: R25.
44. Chavez, L., J. Jozefczuk, C. Grimm, J. Dietrich, B. Timmermann, H. Lehrach, R. Herwig, and J. Adjaye. 2010. Computational analysis of genome-wide DNA methylation during the differentiation of human embryonic stem cells along the endodermal lineage. Genome Res. 20: 1441-1450.
45. Robinson, M. D., D. J. McCarthy, and G. K. Smyth. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
46. Morgan, M. 2010. An introduction to Rsamtools . Available at: http://www.bioconductor.org/help/course-materials/2015/LearnBioconductorFeb2015/. Accessed: March 10, 2015.
47. Trapnell, C., A. Roberts, L. Goff, G. Pertea, D. Kim, D. R. Kelley, H. Pimentel, S. L. Salzberg, J. L. Rinn, and L. Pachter. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7: 562-578.
48. Kaech, S. M., E. J. Wherry, and R. Ahmed. 2002. Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2: 251-262.
49. Wherry, E. J. 2011. T cell exhaustion. Nat. Immunol. 12: 492-499.
50. Singh, K. P., J. A. Bennett, F. L. Casado, J. L. Walrath, S. L. Welle, and T. A. Gasiewicz. 2014. Loss of aryl hydrocarbon receptor promotes gene changes associated with premature hematopoietic stem cell exhaustion and development of a myeloproliferative disorder in aging mice. Stem Cells Dev. 23: 95-106.
51. Boitano, A. E., J. Wang, R. Romeo, L. C. Bouchez, A. E. Parker, S. E. Sutton, J. R. Walker, C. A. Flaveny, G. H. Perdew, M. S. Denison, et al. 2010. Aryl hydrocarbon receptor antagonists promote the expansion of human hematopoietic stem cells. Science 329: 1345-1348.
52. Hu, P., R. Herrmann, A. Bednar, P. Saloupis, M. A. Dwyer, P. Yang, X. Qi, R. S. Thomas, G. J. Jaffe, M. E. Boulton, et al. 2013. Aryl hydrocarbon receptor deficiency causes dysregulated cellular matrix metabolism and age-related macular degeneration-like pathology. Proc. Natl. Acad. Sci. USA 110: E4069-E4078.
53. Jablonska, O., Z. Shi, K. E. Valdez, A. Y. Ting, and B. K. Petroff. 2010. Temporal and anatomical sensitivities to the aryl hydrocarbon receptor agonist 2,3,7,8-tetrachlorodibenzo-p-dioxin leading to premature acyclicity with age in rats. Int. J. Androl. 33: 405-412.
54. Marlowe, J. L., Y. Fan, X. Chang, L. Peng, E. S. Knudsen, Y. Xia, and A. Puga. 2008. The aryl hydrocarbon receptor binds to E2F1 and inhibits E2F1-induced apoptosis. Mol. Biol. Cell 19: 3263-3271.
55. Sartor, M. A., M. Schnekenburger, J. L. Marlowe, J. F. Reichard, Y. Wang, Y. Fan, C. Ma, S. Karyala, D. Halbleib, X. Liu, et al. 2009. Genomewide analysis of aryl hydrocarbon receptor binding targets reveals an extensive array of gene clusters that control morphogenetic and developmental programs. Environ. Health Perspect. 117: 1139-1146.
56. Schietinger, A., J. J. Delrow, R. S. Basom, J. N. Blattman, and P. D. Greenberg. 2012. Rescued tolerant CD8 T cells are preprogrammed to reestablish the tolerant state. Science 335: 723-727.
57. Camacho, I. A., M. Nagarkatti, and P. S. Nagarkatti. 2004. Evidence for induction of apoptosis in T cells from murine fetal thymus following perinatal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicol. Sci. 78: 96-106.
58. Weinstein, D. A., R. M. Gogal, Jr., A. Mustafa, M. R. Prater, and S. D. Holladay. 2008. Mid-gestation exposure of C57BL/6 mice to 2,3,7,8-tetrachlorodibenzo-pdioxin causes postnatal morphologic changes in the spleen and liver. Toxicol. Pathol. 36: 705-713.
59. Bull, C. F., G. Mayrhofer, N. J. O'Callaghan, A. Y. Au, H. A. Pickett, G. K. Low, D. Zeegers, M. P. Hande, and M. F. Fenech. 2014. Folate deficiency induces dysfunctional long and short telomeres; both states are associated with hypomethylation and DNA damage in human WIL2-NS cells. Cancer Prev. Res. (Phila.) 7: 128-138.
60. Li, J., R. A. Harris, S. W. Cheung, C. Coarfa, M. Jeong, M. A. Goodell, L. D. White, A. Patel, S. H. Kang, C. Shaw, et al. 2012. Genomic hypomethylation in the human germline associates with selective structural mutability in the human genome. PLoS Genet. 8: e1002692.
61. Korzeniewski, N., S. Wheeler, P. Chatterjee, A. Duensing, and S. Duensing. 2010. A novel role of the aryl hydrocarbon receptor (AhR) in centrosome amplification - implications for chemoprevention. Mol. Cancer 9: 153.
62. Hochstenbach, K., D. M. van Leeuwen, H. Gmuender, R. W. Gottschalk, S. B. Stølevik, U. C. Nygaard, M. Løvik, B. Granum, E. Namork, H. M. Meltzer, et al. 2012. Toxicogenomic profiles in relation to maternal immunotoxic exposure and immune functionality in newborns. Toxicol. Sci. 129: 315-324.
63. Gomez-Duran, A., E. Ballestar, J. M. Carvajal-Gonzalez, J. L. Marlowe, A. Puga, M. Esteller, and P. M. Fernandez-Salguero. 2008. Recruitment of CREB1 and histone deacetylase 2 (HDAC2) to the mouse Ltbp-1 promoter regulates its constitutive expression in a dioxin receptor-dependent manner. J. Mol. Biol. 380: 1-16.
64. Ovesen, J. L., M. Schnekenburger, and A. Puga. 2011. Aryl hydrocarbon receptor ligands of widely different toxic equivalency factors induce similar histone marks in target gene chromatin. Toxicol. Sci. 121: 123-131.
65. Kurita, H., M. Schnekenburger, J. L. Ovesen, Y. Xia, and A. Puga. 2014. The Ah receptor recruits IKKa to its target binding motifs to phosphorylate serine-10 in histone H3 required for transcriptional activation. Toxicol. Sci. 139: 121-132.
66. Schnekenburger, M., L. Peng, and A. Puga. 2007. HDAC1 bound to the Cyp1a1 promoter blocks histone acetylation associated with Ah receptor-mediated transactivation. Biochim. Biophys. Acta 1769: 569-578.
67. Singh, N. P., U. P. Singh, H. Guan, P. Nagarkatti, and M. Nagarkatti. 2012. Prenatal exposure to TCDD triggers significant modulation of microRNA expression profile in the thymus that affects consequent gene expression. PLoS ONE 7: e45054.
68. Podshivalova, K., and D. R. Salomon. 2013. MicroRNA regulation of T-lymphocyte immunity: modulation of molecular networks responsible for T-cell activation, differentiation, and development. Crit. Rev. Immunol. 33: 435-476.
69. Niedzwiecki, M., H. Zhu, L. Corson, G. Grunig, P. H. Factor, S. Chu, H. Jiang, and R. L. Miller. 2012. Prenatal exposure to allergen, DNA methylation, and allergy in grandoffspring mice. Allergy 67: 904-910.
70. Schaub, B., J. Liu, S. Hoppler, I. Schleich, J. Huehn, S. Olek, G. Wieczorek, S. Illi, and E. von Mutius. 2009. Maternal farm exposure modulates neonatal immune mechanisms through regulatory T cells. J. Allergy Clin. Immunol. 123: 774-782.e5. doi:10.1016/j.jaci.2009.01.056.
71. Fedulov, A. V., and L. Kobzik. 2011. Allergy risk is mediated by dendritic cells with congenital epigenetic changes. Am. J. Respir. Cell Mol. Biol. 44: 285-292.
72. Nguyen, N. T., A. Kimura, T. Nakahama, I. Chinen, K. Masuda, K. Nohara, Y. Fujii-Kuriyama, and T. Kishimoto. 2010. Aryl hydrocarbon receptor negatively regulates dendritic cell immunogenicity via a kynurenine-dependent mechanism. Proc. Natl. Acad. Sci. USA 107: 19961-19966.
73. Simones, T., and D. M. Shepherd. 2011. Consequences of AhR activation in steady-state dendritic cells. Toxicol. Sci. 119: 293-307.