The unexpected role for the aryl hydrocarbon receptor on susceptibility to experimental toxoplasmosis

Journal of Biomedicine and Biotechnology

Volumn 2010, Issue , 2010, Pages

  Sanchez, Yuriko ^a   De Dios Rosado, Juan ^a   Vega, Libia ^b   Elizondo, Guillermo ^b   Estrada Muñiz, Elizabeth ^b   Saavedra, Rafael ^c   Júarez, Imelda ^a   Rodríguez Sosa, Miriam ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

^c INSTITUTO DE INVESTIGACIONES BIOMÉDICAS   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; GAMMA INTERFERON; IMMUNOGLOBULIN E; INTERLEUKIN 10; INTERLEUKIN 12; NITRIC OXIDE; TRANSCRIPTION FACTOR GATA 3; TUMOR NECROSIS FACTOR ALPHA; GATA3 PROTEIN, MOUSE; INTERLEUKIN DERIVATIVE; LIPOXIN; LIPOXIN A; MESSENGER RNA; PARASITE ANTIGEN; SOLUBLE TACHYZOITE ANTIGEN, TOXOPLASMA GONDII;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; IMMUNOGLOBULIN BLOOD LEVEL; INFECTION SENSITIVITY; LIVER INJURY; MALE; MOUSE; NONHUMAN; PERITONEAL EXUDATE CELL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPLEEN CELL; TOXOPLASMA GONDII; TOXOPLASMOSIS; ANIMAL; ASCITES FLUID; BIOSYNTHESIS; BLOOD; BRAIN; C57BL MOUSE; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; INBREEDING; INNATE IMMUNITY; LIVER; METABOLISM; MOUSE MUTANT; PATHOLOGY; SPLEEN; TOXOPLASMA;

MUS; TOXOPLASMA GONDII;

ANIMALS; ANTIGENS, PROTOZOAN; ASCITIC FLUID; BRAIN; FEMALE; FLOW CYTOMETRY; GATA3 TRANSCRIPTION FACTOR; IMMUNITY, INNATE; INBREEDING; INTERFERON-GAMMA; INTERLEUKINS; LIPOXINS; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, ARYL HYDROCARBON; RNA, MESSENGER; SPLEEN; TOXOPLASMA; TOXOPLASMOSIS, ANIMAL; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77950366780     PISSN: 11107243     EISSN: 11107251     Source Type: Journal    
DOI: 10.1155/2010/505694     Document Type: Article

References (63)

1. J. P. Whitlock Jr., "Induction of cytochrome P4501A1," Annual Review of Pharmacology and Toxicology, vol. 39, pp. 103-125, 1999. (Pubitemid 29222553)
2. M. S. Denison and S. R. Nagy, "Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals," Annual Review of Pharmacology and Toxicology, vol. 43, pp. 309-334, 2003. (Pubitemid 37372644)
3. Z.-W. Lai, C. Hundeiker, E. Gleichmann, and C. Esser, "Cytokine gene expression during ontogeny in murine thymus on activation of the aryl hydrocarbon receptor by 2,3,7,8-tetrachlorodibenzo-p-dioxin," Molecular Pharmacology, vol. 52, no. 1, pp. 30-37, 1997. (Pubitemid 27318615)
4. B. A. Jensen, R. J. Leeman, J. J. Schlezinger, and D. H. Sherr, "Aryl hydrocarbon receptor (AhR) agonists suppress interleukin-6 expression by bone marrow stromal cells: an immunotoxicology study," Environmental Health, vol. 2, article 1, pp. 1-13, 2003. (Pubitemid 38813911)
5. M. N'Diaye, E. Le Ferrec, D. Lagadic-Gossmann, et al., "Aryl hydrocarbon receptor-and calcium-dependent induction of the chemokine CCL1 by the environmental contaminant benzo[a]pyrene," Journal of Biological Chemistry, vol. 281, no. 29, pp. 19906-19915, 2006. (Pubitemid 44065764)
6. C. F. A. Vogel, E. Sciullo, P. Wong, P. Kuzmicky, N. Kado, and F. Matsumura, "Induction of proinflammatory cytokines and C-reative protein in human macrophage cell line U937 exposed to air pollution particulates," Environmental Health Perspectives, vol. 113, no. 11, pp. 1536-1541, 2005. (Pubitemid 41614908)
7. T. K. Warren, K. A. Mitchell, and B. P. Lawrence, "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," Toxicological Sciences, vol. 56, no. 1, pp. 114-123, 2000. (Pubitemid 30441470)
8. M.-S. Jeon and C. Esser, "The murine IL-2 promoter contains distal regulatory elements responsive to the Ah receptor, a member of the evolutionarily conserved bHLH-PAS transcription factor family," Journal of Immunology, vol. 165, no. 12, pp. 6975-6983, 2000. (Pubitemid 32001169)
9. J.-H. Yang, C. Vogel, and J. Abel, "A malignant transformation of human cells by 2,3,7,8-tetrachlorodibenzo-p-dioxin exhibits altered expressions of growth regulatory factors," Carcinogenesis, vol. 20, no. 1, pp. 13-18, 1999. (Pubitemid 29033839)
10. T. Negishi, Y. Kato, O. Ooneda, et al., "Effects of aryl hydrocarbon receptor signaling on the modulation of Th1/Th2 balance," Journal of Immunology, vol. 175, no. 11, pp. 7348-7356, 2005. (Pubitemid 41713431)
11. M. S. Denison, A. Pandini, S. R. Nagy, E. P. Baldwin, and L. Bonati, "Ligand binding and activation of the Ah receptor," Chemico-Biological Interactions, vol. 141, no. 1-2, pp. 3-24, 2002. (Pubitemid 35229988)
12. Y.-Z. Gu, J. B. Hogenesch, and C. A. Bradfield, "The PAS superfamily: sensors of environmental and developmental signals," Annual Review of Pharmacology and Toxicology, vol. 40, pp. 519-561, 2000. (Pubitemid 30340692)
13. B. L. Taylor and I. B. Zhulin, "PAS domains: internal sensors of oxygen, redox potential, and light," Microbiology and Molecular Biology Reviews, vol. 63, no. 2, pp. 479-506, 1999. (Pubitemid 29264980)
14. R. Villalobos-Molina, F. G. Vázquez-Cuevas, J. J. López-Guerrero, et al., "Vascular α1D-adrenoceptors are overex-pressed in aorta of the aryl hydrocarbon receptor null mouse: role of increased angiotensin II," Autonomic and Autacoid Pharmacology, vol. 28, no. 2-3, pp. 61-67, 2008. (Pubitemid 351985549)
15. M. Rodróguez-Sosa, G. Elizondo, R. M. López-Durán, I. Rivera, F. J. Gonzalez, and L. Vega, "Over-production of IFN-γ and IL-12 in AhR-null mice," FEBS Letters, vol. 579, no. 28, pp. 6403-6410, 2005. (Pubitemid 41612159)
16. P. Fernandez-Salguero, T. Pineau, D. M. Hilbert, et al., "Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor," Science, vol. 268, no. 5211, pp. 722-726, 1995.
17. C. Esser, A. Rannug, and B. Stockinger, "The aryl hydrocarbon receptor in immunity," Trends in Immunology, vol. 30, no. 9, pp. 447-454, 2009.
18. B. Jux, S. Kadow, and C. Esser, "Langerhans cell maturation and contact hypersensitivity are impaired in aryl hydrocarbon receptor-null mice," Journal of Immunology, vol. 182, no. 11, pp. 6709-6717, 2009.
19. M. Veldhoen, K. Hirota, A. M. Westendorf, et al., "The aryl hydrocarbon receptor links TH17-cell-mediated autoimmu-nity to environmental toxins," Nature, vol. 453, no. 7191, pp. 106-109, 2008. (Pubitemid 351630329)
20. B. P. Lawrence and B. A. Vorderstrasse, "Activation of the aryl hydrocarbon receptor diminishes the memory response to homotypic influenza virus infection but does not impair host resistance," Toxicological Sciences, vol. 79, no. 2, pp. 304-314, 2004. (Pubitemid 38786888)
21. B. A. Vorderstrasse and B. P. Lawrence, "Protection against lethal challenge with Streptococcus pneumoniae is conferred by aryl hydrocarbon receptor activation but is not associated with an enhanced inflammatory response," Infection and Immunity, vol. 74, no. 10, pp. 5679-5686, 2006. (Pubitemid 44484551)
22. L. Z. Shi, N. G. Faith, Y. Nakayama, M. Suresh, H. Steinberg, and C. J. Czuprynski, "The aryl hydrocarbon receptor is required for optimal resistance to Listeria monocytogenes infection in mice," Journal of Immunology, vol. 179, no. 10, pp. 6952-6962, 2007.
23. E. Y. Denkers and R. T. Gazzinelli, "Regulation and function of T-cell-mediated immunity during Toxoplasma gondii infection," Clinical Microbiology Reviews, vol. 11, no. 4, pp. 569-588, 1998. (Pubitemid 28497562)
24. L. A. Lieberman and C. A. Hunter, "The role of cytokines and their signaling pathways in the regulation of immunity to Toxoplasma gondii," International Reviews of Immunology, vol. 21, no. 4-5, pp. 373-403, 2002.
25. T. Scharton-Kersten, E. Y. Denkers, R. Gazzinelli, and A. Sher, "Role of IL12 in induction of cell-mediated immunity to Toxoplasma gondii," Research in Immunology, vol. 146, no. 7-8, pp. 539-545, 1995. (Pubitemid 26054849)
26. G. S. Yap and A. Sher, "Cell-mediated immunity to Toxoplasma gondii: initiation, regulation and effector function," Immuno-biology, vol. 201, no. 2, pp. 240-247, 1999.
27. A. Sher, I. P. Oswald, S. Hieny, and R. T. Gazzinelli, "To x-oplasma gondii induces a T-independent IFN-γ response in natural killer cells that requires both adherent accessory cells and tumor necrosis factor-α," Journal of Immunology, vol. 150, no. 9, pp. 3982-3989, 1993. (Pubitemid 23129780)
28. + T lymphocytes in IFN-γ production and protective immunity induced by an attenuated Toxoplasma gondii vaccine," Journal of Immunology, vol. 146, no. 1, pp. 286-292, 1991.
29. M. Flores, R. Saavedra, R. Bautista, et al., "Macrophage migration inhibitory factor (MIF) is critical for the host resistance against Toxoplasma gondii," FASEB Journal, vol. 22, no. 10, pp. 3661-3671, 2008.
30. T. M. Scharton-Kersten, G. Yap, J. Magram, and A. Sher, "Inducible nitric oxide is essential for host control of persistent but not acute infection with the intracellular pathogen Toxoplasma gondii," Journal of Experimental Medicine, vol. 185, no. 7, pp. 1261-1273, 1997. (Pubitemid 27172907)
31. R. T. Gazzinelli, S. Hieny, T. A. Wynn, S. Wolf, and A. Sher, "Interleukin 12 is required for the T-lymphocyte-independent induction of interferon γ by an intracellular parasite and induces resistance in T-cell-deficient hosts," Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 13, pp. 6115-6119, 1993. (Pubitemid 23191465)
32. T. Fukao, D. M. Frucht, G. Yap, M. Gadina, J. J. O'Shea, and S. Koyasu, "Inducible expression of Stat4 in dendritic cells and macrophages and its critical role in innate and adaptive immune responses," Journal of Immunology, vol. 166, no. 7, pp. 4446-4455, 2001. (Pubitemid 32233728)
33. J. Aliberti, S. Hieny, C. Reis e Sousa, C. N. Serhan, and A. Sher, "Lipoxin-mediated inhibition of IL-12 production by DCs: a mechanism for regulation of microbial immunity," Nature Immunology, vol. 3, no. 1, pp. 76-82, 2002. (Pubitemid 34065621)
34. R. Saavedra, R. Leyva, E. P. Tenorio, et al., "CpG-containing ODN has a limited role in the protection against Toxoplasma gondii," Parasite Immunology, vol. 26, no. 2, pp. 67-73, 2004. (Pubitemid 38916336)
35. W. L. Homan, M. Vercammen, J. de Braekeleer, and H. Verschueren, "Identification of a 200-to 300-fold repetitive 529 bp DNA fragment in Toxoplasma gondii, and its use for diagnostic and quantitative PCR," International Journal for Parasitology, vol. 30, no. 1, pp. 69-75, 2000. (Pubitemid 30089725)
36. G. C. Ulett, N. Ketheesan, and R. G. Hirst, "Cytokine gene expression in innately susceptible BALB/c mice and relatively resistant C57BL/6 mice during infection with virulent Burkholderia pseudomallei" Infection and Immunity, vol. 68, no. 4, pp. 2034-2042, 2000. (Pubitemid 30164834)
37. L. I. Terrazas, D. Montero, C. A. Terrazas, J. L. Reyes, and M. Rodróguez-Sosa, "Role of the programmed death-1 pathway in the suppressive activity of alternatively activated macrophages in experimental cysticercosis," International Journal for Parasitology, vol. 35, no. 13, pp. 1349-1358, 2005. (Pubitemid 41484148)
38. Q. Tong, G. Dalgin, H. Xu, C.-N. Ting, J. M. Leiden, and G. S. Hotamisligil, "Function of GATA transcription factors in preadipocyte-adipocyte transition," Science, vol. 290, no. 5489, pp. 134-138, 2000.
39. G. Bonizzi, J. Piette, M.-P Merville, and V. Bours, "Distinct signal transduction pathways mediate nuclear factor-kB induction by IL-1/3 in epithelial and lymphoid cells," Journal of Immunology, vol. 159, no. 11, pp. 5264-5272, 1997. (Pubitemid 127470052)
40. M. Renshaw, J. Rockwell, C. Engleman, A. Gewirtz, J. Katz, and S. Sambhara, "Cutting edge: impaired toll-like receptor expression and function in aging," Journal of Immunology, vol. 169, no. 9, pp. 4697-4701, 2002. (Pubitemid 35217128)
41. M. Rodróguez-Sosa, L. E. Rosas, J. R. David, R. Bojalil, A. R. Satoskar, and L. I. Terrazas, "Macrophage migration inhibitory factor plays a critical role in mediating protection against the helminth parasite Taenia crassiceps" Infection and Immunity, vol. 71, no. 3, pp. 1247-1254, 2003. (Pubitemid 36254308)
42. J. L. Reyes, L. I. Terrazas, B. Espinoza, et al., "Macrophage migration inhibitory factor contributes to host defense against acute Trypanosoma cruzi infection," Infection and Immunity, vol. 74, no. 6, pp. 3170-3179, 2006. (Pubitemid 43794505)
43. D. L. Granger, R. R. Taintor, K. S. Boockvar, and J. B. Hibbs Jr., "Measurement of nitrate and nitrite in biological samples using nitrate reductase and Griess reaction," Methods in Enzymology, vol. 268, pp. 142-151, 1996. (Pubitemid 26286356)
44. P. Migliorini, G. Corradin, and S. B. Corradin, "Macrophage NO2 ̄ production as a sensitive and rapid assay for the quantitation of murine IFN-y," Journal of Immunological Methods, vol. 139, no. 1, pp. 107-114, 1991.
45. G. Trinchieri, "Interleukin-12: a cytokine at the interface of inflammation and immunity," Advances in Immunology, vol. 70, pp. 83-243, 1998. (Pubitemid 128678837)
46. G. Yap, M. Pesin, and A. Sher, "Cutting edge: IL-12 is required for the maintenance of IFN-y production in T cells mediating chronic resistance to the intracellular pathogen, Toxoplasma gondii," Journal of Immunology, vol. 165, no. 2, pp. 628-631, 2000. (Pubitemid 30484726)
47. + dendritic cells," Nature Immunology, vol. 1, no. 1, pp. 83-87, 2000.
48. F. S. Machado, J. E. Johndrow, L. Esper, et al., "Anti-inflammatory actions of lipoxin A4 and aspirin-triggered lipoxin are SOCS-2 dependent," Nature Medicine, vol. 12, no. 3, pp. 330-334, 2006. (Pubitemid 43355082)
49. B. A. Vorderstrasse, J. A. Cundiff, and B. P. Lawrence, "A dose-response study of the effects of prenatal and lactational exposure to TCDD on the immune response to influenza A virus," Journal of Toxicology and Environmental Health A, vol. 69, no. 6, pp. 445-463, 2006.
50. Y. Suzuki, M. A. Orellana, R. D. Schreiber, and J. S. Remington, "Interferon-γ: the major mediator of resistance against To x o-plasma gondii," Science, vol. 240, no. 4851, pp. 516-518, 1988.
51. U. Gross, O. Keksel, and M. L. Dardé, "Value of detecting immunoglobulin E antibodies for the serological diagnosis of Toxoplasma gondii infection," Clinical and Diagnostic Laboratory Immunology, vol. 4, no. 3, pp. 247-251, 1997. (Pubitemid 27239678)
52. J. Matowicka-Karna, V. Dymicka-Piekarska, and H. Kemona, "Does Toxoplasma gondii infection affect the levels of IgE and cytokines (IL-5, IL-6, IL-10, IL-12, and TNF-alpha)?" Clinical and Developmental Immunology, vol. 2009, Article ID 374696, 4 pages, 2009.
53. I. A. Khan, J. D. Schwartzman, T. Matsuura, and L. H. Kasper, "A dichotomous role for nitric oxide during acute To x o p l a s m a gondii infection in mice," Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 25, pp. 13955-13960, 1997. (Pubitemid 28009691)
54. Y. Suzuki, A. Sher, G. Yap, et al., "IL-10 is required for prevention of necrosis in the small intestine and mortality in both genetically resistant BALB/c and susceptible C57BL/6 mice following peroral infection with Toxoplasma gondii," Journal of Immunology, vol. 164, no. 10, pp. 5375-5382, 2000. (Pubitemid 30305218)
55. 2/M phases in aryl hydrocarbon receptor-null embryo fibroblast," Molecular Pharmacology, vol. 57, no. 5, pp. 1056-1063, 2000. (Pubitemid 30253392)
56. + cells with characteristics of regulatory T cells," Journal of Immunology, vol. 175, no. 7, pp. 4184-4188, 2005. (Pubitemid 41361950)
57. F. Yarovinsky and A. Sher, "Toll-like receptor recognition of Toxoplasma gondii," International Journal for Parasitology, vol. 36, no. 3, pp. 255-259, 2006. (Pubitemid 43376107)
58. H.-S. Mun, F. Aosai, K. Norose, et al., "TLR2 as an essential molecule for protective immunity against Toxoplasma gondii infection," International Immunology, vol. 15, no. 9, pp. 1081-1087, 2003. (Pubitemid 37063207)
59. S. Chamorro, J. J. García-Vallejo, W. W. Unger, et al., "TLR triggering on tolerogenic dendritic cells results in TLR2 up-regulation and a reduced proinflammatory immune program," Journal of Immunology, vol. 183, no. 5, pp. 2984-2994, 2009.
60. M. G. Netea, R. Sutmuller, C. Hermann, et al., "Toll-like receptor 2 suppresses immunity against Candida albicans through induction of IL-10 and regulatory T cells," Journal of Immunology, vol. 172, no. 6, pp. 3712-3718, 2004. (Pubitemid 38337955)
61. Y. Yanagawa and K. Onoé, "Enhanced IL-10 production by TLR4-and TLR2-primed dendritic cells upon TLR restimula-tion," Journal of Immunology, vol. 178, no. 10, pp. 6173-6180, 2007. (Pubitemid 46717399)
62. C. M. Schaldach, J. Riby, and L. F. Bjeldanes, "Lipoxin A4: a new class of ligand for the Ah receptor," Biochemistry, vol. 38, no. 23, pp. 7594-7600, 1999.
63. J. Aliberti, C. Serhan, and A. Sher, "Parasite-induced lipoxin A4 is an endogenous regulator of IL-12 production and immunopathology in Toxoplasma gondii infection," Journal of Experimental Medicine, vol. 196, no. 9, pp. 1253-1262, 2002. (Pubitemid 35304190)