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

Molecular Pharmacology

Volumn 73, Issue 6, 2008, Pages 1722-1735

  Singh, Narendra P ^a   Nagarkatti, Mitzi ^a   Nagarkatti, Prakash S ^a  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; CONCANAVALIN A; FAS LIGAND; FLICE INHIBITORY PROTEIN; OVALBUMIN; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; C57BL 6 MOUSE; CELL CULTURE; CELL MATURATION; CYTOTOXICITY; DENDRITIC CELL; DOWN REGULATION; IN VITRO STUDY; MOUSE; MOUSE STRAIN; NONHUMAN; OT.II.2A MOUSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; UPREGULATION;

ANIMALS; APOPTOSIS; CELLS, CULTURED; DENDRITIC CELLS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; T-LYMPHOCYTE SUBSETS; TETRACHLORODIBENZODIOXIN;

EID: 44249086903     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.107.043406     Document Type: Article

References (49)

1. Bock KW and Kohle C (2006) Ah receptor: dioxin-mediated toxic responses as hints to deregulated physiologic functions. Biochem Pharmacol 72:393-404.
2. Camacho IA, Hassuneh MR, Nagarkatti M, and Nagarkatti PS (2001) Enhanced activation-induced cell death as a mechanism of 2,3,7,8-tetrachlorodibenzo-p- dioxin (TCDD)-induced immunotoxicity in peripheral T cells. Toxicology 165:51-63.
3. Camacho IA, Nagarkatti M, and Nagarkatti PS (2002) 2,3,7,8- Tetrachlorodibenzo-p-dioxin (TCDD) induces Fas-dependent activation-induced cell death in superantigen-primed T cells. Arch Toxicol 76:570-580.
4. Camacho IA, Nagarkatti M, and Nagarkatti PS (2004a) Effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on maternal immune response during pregnancy. Arch Toxicol 78:290-300.
5. Camacho IA, Nagarkatti M, and Nagarkatti PS (2004b) 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.
6. Camacho IA, Singh N, Hegde VL, Nagarkatti M, and Nagarkatti PS (2005) Treatment of mice with 2,3,7,8-tetrachlorodibenzo-p-dioxin leads to aryl hydrocarbon receptor-dependent nuclear translocation of NF-kappaB and expression of fas ligand in thymic stromal cells and consequent apoptosis in T cells. J Immunol 175:90-103.
7. Dertinger SD, Nazarenko DA, Silverstone AE, and Gasiewicz TA (2001) Aryl hydrocarbon receptor signaling plays a significant role in mediating benzo[a]pyrene- and cigarette smoke condensate-induced cytogenetic damage in vivo. Carcinogenesis 22:171-177.
8. Do Y, Hegde VL, Nagarkatti PS, and Nagarkatti M (2004a) Bryostatin-1 enhances the maturation and antigen-presenting ability of murine and human dendritic cells. Cancer Res 64:6756-6765.
9. Do Y, McKallip RJ, Nagarkatti M, and Nagarkatti PS (2004b) Activation through cannabinoid receptors 1 and 2 on dendritic cells triggers NF-kappaB-dependent apoptosis: novel role for endogenous and exogenous cannabinoids in immunoregulation. J Immunol 173:2373-2382.
10. Esser C (1994) Dioxins and the immune system: mechanisms of interference. A meeting report. Int Arch Allergy Immunol 104:126-130.
11. Faith RE and Luster MI (1979) Investigations on the effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on parameters of various immune functions. Ann N Y Acad Sci 320:564-571.
12. Fernandez-Salguero PM, Hilbert DM, Rudikoff S, Ward JM, and Gonzalez FJ (1996) Aryl-hydrocarbon receptor-deficient mice are resistant to 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced toxicity. Toxicol Appl Pharmacol 140:173-179.
13. Fikri Y, Pastoret PP, and Nyabenda J (2002) Costimulatory molecule requirement for bovine WC1+gammadelta T cells' proliferative response to bacterial superantigens. Scand J Immunol 55:373-381.
14. Fine JS, Gasiewicz TA, Fiore NC, and Silverstone AE (1990) Prothymocyte activity is reduced by perinatal 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure. J Pharmacol Exp Ther 255:128-132.
15. Golks A, Brenner D, Fritsch C, Krammer PH, and Lavrik IN (2005) c-FLIPR, a new regulator of death receptor-induced apoptosis. J Biol Chem 280:14507-14513.
16. Gonzalez FJ and Fernandez-Salguero P (1998) The aryl hydrocarbon receptor: studies using the AHR-null mice. Drug Metab Dispos 26:1194-1198.
17. Greenlee WF, Dold KM, and Osborne R (1985) Actions of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on human epidermal keratinocytes in culture. In Vitro Cell Dev Biol 21:509-512.
18. Harper PA, Riddick DS, and Okey AB (2006) Regulating the regulator: factors that control levels and activity of the aryl hydrocarbon receptor. Biochem Pharmacol 72:267-279.
19. Holladay SD, Brownie CF, Corbett WT, and Talley DD (1991) Evaluation of an indirect enzyme-linked immunosorbent assay for screening antibody against aflatoxins. Am J Vet Res 52:222-223.
20. Hossain A, Tsuchiya S, Minegishi M, Osada M, Ikawa S, Tezuka FA, Kaji M, Konno T, Watanabe M, and Kikuchi H (1998) The Ah receptor is not involved in 2,3,7,8-tetrachlorodibenzo-p-dioxin-mediated apoptosis in human leukemic T cell lines. J Biol Chem 273:19853-19858.
21. Kamath AB, Camacho I, Nagarkatti PS, and Nagarkatti M (1999) Role of Fas-Fas ligand interactions in 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-induced immunotoxicity: increased resistance of thymocytes from Fas-deficient (lpr) and Fas ligand-defective (gld) mice to TCDD-induced toxicity. Toxicol Appl Pharmacol 160:141-155.
22. Kamath AB, Xu H, Nagarkatti PS, and Nagarkatti M (1997) Evidence for the induction of apoptosis in thymocytes by 2,3,7,8-tetrachlorodibenzo-p-dioxin in vivo. Toxicol Appl Pharmacol 142:367-377.
23. Kerkvliet NI (2002) Recent advances in understanding the mechanisms of TCDD immunotoxicity. Int Immunopharmacol 2:277-291.
24. Kerkvliet NI, Shepherd DM, and Baecher-Steppan L (2002) T lymphocytes are direct, aryl hydrocarbon receptor (AhR)-dependent targets of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD): AhR expression in both CD4+ and CD8+ T cells is necessary for full suppression of a cytotoxic T lymphocyte response by TCDD. Toxicol Appl Pharmacol 185:146-152.
25. Lavrik IN, Golks A, and Krammer PH (2005a) Caspases: pharmacological manipulation of cell death. J Clin Invest 115:2665-2672.
26. Lavrik I, Golks A, and Krammer PH (2005b) Death receptor signaling. J Cell Sci 118:265-267.
27. Lundberg K, Dencker L, and Gronvik KO (1990a) Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) treatment in vivo on thymocyte functions in mice after activation in vitro. Int J Immunopharmacol 12:459-466.
28. Lundberg K, Dencker L, and Gronvik KO (1992) 2,3,7,8-Tetrachlorodibenzo- p-dioxin (TCDD) inhibits the activation of antigen-specific T-cells in mice. Int J Immunopharmacol 14:699-705.
29. Lundberg K, Gronvik KO, Goldschmidt TJ, Klareskog L, and Dencker L (1990b) 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) alters intrathymic T-cell development in mice. Chem Biol Interact 74:179-193.
30. Marlowe JL and Puga A (2005) Aryl hydrocarbon receptor, cell cycle regulation, toxicity, and tumorigenesis. J Cell Biochem 96:1174-1184.
31. Matikainen T, Perez GI, Jurisicova A, Pru JK, Schlezinger JJ, Ryu HY, Laine J, Sakai T, Korsmeyer SJ, Casper RF, et al. (2001) Aromatic hydrocarbon receptor-driven Bax gene expression is required for premature ovarian failure caused by biohazardous environmental chemicals. Nat Genet 28:355-360.
32. Mimura J and Fujii-Kuriyama Y (2003) [Xenobiotics and transcriptional regulation]. Tanpakushitsu Kakusan Koso 48:2261-2266.
33. Nagarkatti PS, Sweeney GD, Gauldie J, and Clark DA (1984) Sensitivity to suppression of cytotoxic T cell generation by 2,3,7,8-tetrachlorodibenzo-p- dioxin (TCDD) is dependent on the Ah genotype of the murine host. Toxicol Appl Pharmacol 72: 169-176.
34. Nazarenko DA, Dertinger SD, and Gasiewicz TA (2001) In vivo antagonism of AhR-mediated gene induction by 3′-methoxy-4′-nitroflavone in TCDD-responsive lacZ mice. Toxicol Sci 61:256-264.
35. O'Connell PJ, Morelli AE, Logar AJ, and Thomson AW (2000) Phenotypic and functional characterization of mouse hepatic CD8 alpha+ lymphoid-related dendritic cells. J Immunol 165:795-803.
36. Palao G, Santiago B, Galindo M, Paya M, Ramirez JC, and Pablos JL (2004) Down-regulation of FLIP sensitizes rheumatoid synovial fibroblasts to Fasmediated apoptosis. Arthritis Rheum 50:2803-2810.
37. Park JH, Hahn EJ, Kong JH, Cho HJ, Yoon CS, Cheong SW, Oh GS, and Youn HJ (2003) TCDD-induced apoptosis in EL-4 cells deficient of the aryl hydrocarbon receptor and down-regulation of IGFBP-6 prevented the apoptotic cell death. Toxicol Lett 145:55-68.
38. Pryputniewicz SJ, Nagarkatti M, and Nagarkatti PS (1998) Differential induction of apoptosis in activated and resting T cells by 2,3,7,8- tetrachlorodibenzo-p-dioxin (TCDD) and its repercussion on T cell responsiveness. Toxicology 129:211-226.
39. Rhile MJ, Nagarkatti M, and Nagarkatti PS (1996) Role of Fas apoptosis and MHC genes in 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-induced immunotoxicity of T cells. Toxicology 110:153-167.
40. Salon C, Eymin B, Micheau O, Chaperot L, Plumas J, Brambilla C, Brambilla E, and Gazzeri S (2006) E2F1 induces apoptosis and sensitizes human lung adenocarcinoma cells to death-receptor-mediated apoptosis through specific downregulation of c-FLIP(short). Cell Death Differ 13:260-272.
41. Schmidt JV and Bradfield CA (1996) Ah receptor signaling pathways. Annu Rev Cell Dev Biol 12:55-89.
42. Singh NP, Nagarkatti M, and Nagarkatti PS (2007) Role of dioxin response element and nuclear factor-kappaB motifs in 2,3,7,8-tetrachlorodibenzo-p-dioxin- mediated regulation of Fas and Fas ligand expression. Mol Pharmacol 71:145-157.
43. Strauss G, Knape I, Melzner I, and Debatin KM (2003) Constitutive caspase activation and impaired death-inducing signaling complex formation in CD95-resistant, long-term activated, antigen-specific T cells. J Immunol 171:1172-1182.
44. Suhara T, Mano T, Oliveira BE, and Walsh K (2001) Phosphatidylinositol 3-kinase/Akt signaling controls endothelial cell sensitivity to Fas-mediated apoptosis via regulation of FLICE-inhibitory protein (FLIP). Circ Res 89:13-19.
45. Sulentic CE, Holsapple MP, and Kaminski NE (2000) Putative link between transcriptional regulation of IgM expression by 2,3,7,8-tetrachlorodibenzo-p- dioxin and the aryl hydrocarbon receptor/dioxin-responsive enhancer signaling pathway. J Pharmacol Exp Ther 295:705-716.
46. Tian Y, Ke S, Denison MS, Rabson AB, and Gallo MA (1999) Ah receptor and NF-κB interactions, a potential mechanism for dioxin toxicity. J Biol Chem 274:510-515.
47. Tran SE, Meinander A, Holmstrom TH, Rivero-Muller A, Heiskanen KM, Linnau EK, Courtney MJ, Mosser DD, Sistonen L, and Eriksson JE (2003) Heat stress downregulates FLIP and sensitizes cells to Fas receptor-mediated apoptosis. Cell Death Differ 10:1137-1147.
48. Uriarte SM, Joshi-Barve S, Song Z, Sahoo R, Gobejishvili L, Jala VR, Haribabu B, McClain C, and Barve S (2005) Akt inhibition upregulates FasL, downregulates c-FLIPs and induces caspase-8-dependent cell death in Jurkat T lymphocytes. Cell Death Differ 12:233-242.
49. Whitlock JP Jr (1999) Induction of cytochrome P4501A1. Annu Rev Pharmacol Toxicol 39:103-125.