A single mid-gestation exposure to TCDD yields a postnatal autoimmune signature, differing by sex, in early geriatric C57BL/6 mice

Toxicology

Volumn 290, Issue 2-3, 2011, Pages 156-168

  Mustafa, A ^a   Holladay, S D ^b   Witonsky, S ^a   Sponenberg, D P ^a   Karpuzoglu, E ^b   Gogal, R M ^b  

^a VIRGINIA MARYLAND REGIONAL COLLEGE OF VETERINARY MEDICINE   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

Autoimmunity; B cell; Bone marrow; C57BL 6 mice; T cell; TCDD

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AUTOANTIBODY; CARDIOLIPIN; CD1 ANTIGEN; CD23 ANTIGEN; CD24 ANTIGEN; COMPLEMENT COMPONENT C3D RECEPTOR; DOUBLE STRANDED DNA; GAMMA INTERFERON; INTERLEUKIN 10; SINGLE STRANDED DNA; SYNDECAN 1; CARDIOLIPIN ANTIBODY;

AGE DISTRIBUTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; DISSOCIATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MOUSE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; SEX DIFFERENCE; SPLEEN CELL; T LYMPHOCYTE ACTIVATION; AGE; ANIMAL; AUTOIMMUNE DISEASE; B LYMPHOCYTE; C57BL MOUSE; CHEMICALLY INDUCED DISORDER; CYTOLOGY; IMMUNOLOGY; POLLUTANT; PRENATAL EXPOSURE; SPLEEN; T LYMPHOCYTE;

MUS;

AGE FACTORS; ANIMALS; ANTIBODIES, ANTICARDIOLIPIN; AUTOANTIBODIES; AUTOIMMUNE DISEASES; B-LYMPHOCYTES; ENVIRONMENTAL POLLUTANTS; FEMALE; INTERFERON-GAMMA; INTERLEUKIN-10; MALE; MICE; MICE, INBRED C57BL; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SEX FACTORS; SPLEEN; SYNDECAN-1; T-LYMPHOCYTES; TETRACHLORODIBENZODIOXIN;

EID: 84858615530     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2011.08.021     Document Type: Article

References (91)

1. Allman D., Pillai S. Peripheral B cell subsets. Curr. Opin. Immunol. 2008, 20:149-157.
2. Bagavant H., Deshmukh U.S., Gaskin F., Fu S.M. Lupus glomerulonephritis revisited 2004: autoimmunity and end-organ damage. Scand. J. Immunol. 2004, 60:52-63.
3. Batten M., Groom J., Cachero T.G., Qian F., Schneider P., Tschopp J., Browning J.L., Mackay F. BAFF mediates survival of peripheral immature B lymphocytes. J. Exp. Med. 2000, 192:1453-1466.
4. Belostocki K.B., Paget S.A. Inflammatory rheumatologic disorders in the elderly. Unusual presentations, altered outlooks. Postgrad. Med. 2002, 111. 72-74, 77-78, 81-73.
5. Billiau A. Interferon-gamma in autoimmunity. Cytokine Growth Factor Rev. 1996, 7:25-34.
6. Blaylock B.L., Holladay S.D., Comment C.E., Heindel J.J., Luster M.I. Exposure to tetrachlorodibenzo-p-dioxin (TCDD) alters fetal thymocyte maturation. Toxicol. Appl. Pharmacol. 1992, 112:207-213.
7. Boddaert J., Huong D.L., Amoura Z., Wechsler B., Godeau P., Piette J.C. Late-onset systemic lupus erythematosus: a personal series of 47 patients and pooled analysis of 714 cases in the literature. Medicine (Baltimore) 2004, 83:348-359.
8. Boren E., Gershwin M.E. Inflamm-aging: autoimmunity, and the immune-risk phenotype. Autoimmun. Rev. 2004, 3:401-406.
9. Camacho I.A., Singh N., Hegde V.L., Nagarkatti M., Nagarkatti P.S. 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. 2005, 175:90-103.
10. Campbell I.L., Kay T.W., Oxbrow L., Harrison L.C. Essential role for interferon-gamma and interleukin-6 in autoimmune insulin-dependent diabetes in NOD/Wehi mice. J. Clin. Invest. 1991, 87:739-742.
11. Cancro M.P., Smith S.H. Peripheral B cell selection and homeostasis. Immunol. Res. 2003, 27:141-148.
12. Carnrot C., Prokopec K.E., Rasbo K., Karlsson M.C., Kleinau S. Marginal zone B cells are naturally reactive to collagen type II and are involved in the initiation of the immune response in collagen-induced arthritis. Cell. Mol. Immunol. 2011, 8:296-304.
13. Catoggio L.J., Skinner R.P., Smith G., Maddison P.J. Systemic lupus erythematosus in the elderly: clinical and serological characteristics. J. Rheumatol. 1984, 11:175-181.
14. Cervera R., Khamashta M.A., Font J., Sebastiani G.D., Gil A., Lavilla P., Domenech I., Aydintug A.O., Jedryka-Goral A., de Ramon E., et al. Systemic lupus erythematosus: clinical and immunologic patterns of disease expression in a cohort of 1,000 patients. The European Working Party on Systemic Lupus Erythematosus. Medicine (Baltimore) 1993, 72:113-124.
15. Chang D.M., Chang C.C., Kuo S.Y., Chu S.J., Chang M.L. The clinical features and prognosis of male lupus in Taiwan. Lupus 1998, 7:462-468.
16. Cooper G.S., Parks C.G., Treadwell E.L., St Clair E.W., Gilkeson G.S., Cohen P.L., Roubey R.A., Dooley M.A. Differences by race, sex and age in the clinical and immunologic features of recently diagnosed systemic lupus erythematosus patients in the southeastern United States. Lupus 2002, 11:161-167.
17. de Carvalho J.F., do Nascimento A.P., Testagrossa L.A., Barros R.T., Bonfa E. Male gender results in more severe lupus nephritis. Rheumatol. Int. 2010, 30:1311-1315.
18. Dunn-Walters D.K., Ademokun A.A. B cell repertoire and ageing. Curr. Opin. Immunol. 2010, 22:514-520.
19. Esser C. Dioxins and the immune system: mechanisms of interference. A meeting report. Int. Arch. Allergy Immunol. 1994, 104:126-130.
20. Finch C.E., Crimmins E.M. Inflammatory exposure and historical changes in human life-spans. Science 2004, 305:1736-1739.
21. Fine J.S., Silverstone A.E., Gasiewicz T.A. Impairment of prothymocyte activity by 2,3,7,8-tetrachlorodibenzo-p-dioxin. J. Immunol. 1990, 144:1169-1176.
22. Fine J.S., Gasiewicz T.A., Fiore N.C., Silverstone A.E. Prothymocyte activity is reduced by perinatal 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure. J. Pharmacol. Exp. Ther. 1990, 255:128-132.
23. Fisher M.T., Nagarkatti M., Nagarkatti P.S. Combined screening of thymocytes using apoptosis-specific cDNA array and promoter analysis yields novel gene targets mediating TCDD-induced toxicity. Toxicol. Sci. 2004, 78:116-124.
24. Formiga F., Moga I., Pac M., Mitjavila F., Rivera A., Pujol R. Mild presentation of systemic lupus erythematosus in elderly patients assessed by SLEDAI. SLE Disease Activity Index. Lupus 1999, 8:462-465.
25. Franceschi C., Bonafe M., Valensin S., Olivieri F., De Luca M., Ottaviani E., De Benedictis G. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann. N.Y. Acad. Sci. 2000, 908:244-254.
26. Frericks M., Temchura V.V., Majora M., Stutte S., Esser C. Transcriptional signatures of immune cells in aryl hydrocarbon receptor (AHR)-proficient and AHR-deficient mice. Biol. Chem. 2006, 387:1219-1226.
27. Fujimoto M., Sato S. B cell signaling and autoimmune diseases: CD19/CD22 loop as a B cell signaling device to regulate the balance of autoimmunity. J. Dermatol. Sci. 2007, 46:1-9.
28. Gehrs B.C., Smialowicz R.J. Alterations in the developing immune system of the F344 rat after perinatal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin I [correction of II]. Effects on the fetus and the neonate. Toxicology 1997, 122:219-228.
29. Gehrs B.C., Smialowicz R.J. Persistent suppression of delayed-type hypersensitivity in adult F344 rats after perinatal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicology 1999, 134:79-88.
30. Gogal R.M., Prater M.R., Smith B.J., Johnson M.S., Holladay S.D. Bilateral dissected spleens and thymuses in rodents exhibit homogeneity in leukocyte markers. Toxicology 2001, 157:217-223.
31. Grimaldi C.M., Michael D.J., Diamond B. Cutting edge: expansion and activation of a population of autoreactive marginal zone B cells in a model of estrogen-induced lupus. J. Immunol. 2001, 167:1886-1890.
32. Haas C., Ryffel B., Le Hir M. IFN-gamma is essential for the development of autoimmune glomerulonephritis in MRL/Ipr mice. J. Immunol. 1997, 158:5484-5491.
33. Hagiwara E., Gourley M.F., Lee S., Klinman D.K. Disease severity in patients with systemic lupus erythematosus correlates with an increased ratio of interleukin-10:interferon-gamma-secreting cells in the peripheral blood. Arthritis Rheum. 1996, 39:379-385.
34. Hanawa H., Tsuchida M., Matsumoto Y., Watanabe H., Abo T., Sekikawa H., Kodama M., Zhang S., Izumi T., Shibata A. Characterization of T cells infiltrating the heart in rats with experimental autoimmune myocarditis. Their similarity to extrathymic T cells in mice and the site of proliferation. J. Immunol. 1993, 150:5682-5695.
35. Hashimoto H., Tsuda H., Hirano T., Takasaki Y., Matsumoto T., Hirose S. Differences in clinical and immunological findings of systemic lupus erythematosus related to age. J. Rheumatol. 1987, 14:497-501.
36. Hayashi Y., Haneji N., Hamano H. Cytokine gene expression and autoantibody production in Sjogren's syndrome of MRL/lpr mice. Autoimmunity 1996, 23:269-277.
37. Ho C.T., Mok C.C., Lau C.S., Wong R.W. Late onset systemic lupus erythematosus in southern Chinese. Ann. Rheum. Dis. 1998, 57:437-440.
38. Holladay S.D., Smialowicz R.J. Development of the murine and human immune system: differential effects of immunotoxicants depend on time of exposure. Environ. Health Perspect. 2000, 108(Suppl. 3):463-473.
39. Holladay S.D., Lindstrom P., Blaylock B.L., Comment C.E., Germolec D.R., Heindell J.J., Luster M.I. Perinatal thymocyte antigen expression and postnatal immune development altered by gestational exposure to tetrachlorodibenzo-p-dioxin (TCDD). Teratology 1991, 44:385-393.
40. Holladay S.D., Mustafa A., Gogal R.M. Prenatal TCDD in mice increases adult autoimmunity. Reprod. Toxicol. 2011, 31(3):312-318.
41. Holsapple M.P., Snyder N.K., Wood S.C., Morris D.L. A review of 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced changes in immunocompetence: 1991 update. Toxicology 1991, 69:219-255.
42. Horwitz D.A., Gray J.D., Behrendsen S.C., Kubin M., Rengaraju M., Ohtsuka K., Trinchieri G. Decreased production of interleukin-12 and other Th1-type cytokines in patients with recent-onset systemic lupus erythematosus. Arthritis Rheum. 1998, 41:838-844.
43. Johnson S.A., Rozzo S.J., Cambier J.C. Aging-dependent exclusion of antigen-inexperienced cells from the peripheral B cell repertoire. J. Immunol. 2002, 168:5014-5023.
44. Kamath A.B., Xu H., Nagarkatti P.S., Nagarkatti M. Evidence for the induction of apoptosis in thymocytes by 2,3,7,8-tetrachlorodibenzo-p-dioxin in vivo. Toxicol. Appl. Pharmacol. 1997, 142:367-377.
45. Kaufman L.D., Gomez-Reino J.J., Heinicke M.H., Gorevic P.D. Male lupus: retrospective analysis of the clinical and laboratory features of 52 patients, with a review of the literature. Semin. Arthritis Rheum. 1989, 18:189-197.
46. Klein A.B., Witonsky S.G., Ahmed S.A., Holladay S.D., Gogal R.M., Link L., Reilly C.M. Impact of different cell isolation techniques on lymphocyte viability and function. J. Immunoassay Immunochem. 2006, 27:61-76.
47. Kline G.H., Hayden T.A., Klinman N.R. B cell maintenance in aged mice reflects both increased B cell longevity and decreased B cell generation. J. Immunol. 1999, 162:3342-3349.
48. Klinman N.R., Kline G.H. The B-cell biology of aging. Immunol. Rev. 1997, 160:103-114.
49. Krabbe K.S., Pedersen M., Bruunsgaard H. Inflammatory mediators in the elderly. Exp. Gerontol. 2004, 39:687-699.
50. Lazuardi L., Jenewein B., Wolf A.M., Pfister G., Tzankov A., Grubeck-Loebenstein B. Age-related loss of naive T cells and dysregulation of T-cell/B-cell interactions in human lymph nodes. Immunology 2005, 114:37-43.
51. LeMaoult J., Szabo P., Weksler M.E. Effect of age on humoral immunity, selection of the B-cell repertoire and B-cell development. Immunol. Rev. 1997, 160:115-126.
52. Loder F., Mutschler B., Ray R.J., Paige C.J., Sideras P., Torres R., Lamers M.C., Carsetti R. B cell development in the spleen takes place in discrete steps and is determined by the quality of B cell receptor-derived signals. J. Exp. Med. 1999, 190:75-89.
53. Lundberg K., Dencker L., Gronvik K.O. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) inhibits the activation of antigen-specific T-cells in mice. Int. J. Immunopharmacol. 1992, 14:699-705.
54. Luster M.I., Boorman G.A., Dean J.H., Harris M.W., Luebke R.W., Padarathsingh M.L., Moore J.A. Examination of bone marrow, immunologic parameters and host susceptibility following pre- and postnatal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Int. J. Immunopharmacol. 1980, 2:301-310.
55. Luster M.I., Dean J.H., Germolec D.R. Consensus workshop on methods to evaluate developmental immunotoxicity. Environ. Health Perspect. 2003, 111:579-583.
56. Maddison P.J. Systemic lupus erythematosus in the elderly. J. Rheumatol. Suppl. 1987, 14(Suppl. 13):182-187.
57. Martin F., Chan A.C. B cell immunobiology in disease: evolving concepts from the clinic. Annu. Rev. Immunol. 2006, 24:467-496.
58. Martin F., Kearney J.F. B-cell subsets and the mature preimmune repertoire. Marginal zone and B1 B cells as part of a " natural immune memory" . Immunol. Rev. 2000, 175:70-79.
59. Masten S.A., Shiverick K.T. The Ah receptor recognizes DNA binding sites for the B cell transcription factor, BSAP: a possible mechanism for dioxin-mediated alteration of CD19 gene expression in human B lymphocytes. Biochem. Biophys. Res. Commun. 1995, 212:27-34.
60. McMillan B.J., McMillan S.N., Glover E., Bradfield C.A. 2,3,7,8-Tetrachlorodibenzo-p-dioxin induces premature activation of the KLF2 regulon during thymocyte development. J. Biol. Chem. 2007, 282:12590-12597.
61. Miller R.A. The aging immune system: primer and prospectus. Science 1996, 273:70-74.
62. Monroe J.G., Bannish G., Fuentes-Panana E.M., King L.B., Sandel P.C., Chung J., Sater R. Positive and negative selection during B lymphocyte development. Immunol. Res. 2003, 27:427-442.
63. Mustafa A., Holladay S.D., Goff M., Witonsky S.G., Kerr R., Reilly C.M., Sponenberg D.P., Gogal R.M. An enhanced postnatal autoimmune profile in 24 week-old C57BL/6 mice developmentally exposed to TCDD. Toxicol. Appl. Pharmacol. 2008, 232:51-59.
64. Mustafa A., Holladay S.D., Goff M., Witonsky S., Kerr R., Weinstein D.A., Karpuzoglu-Belgin E., Gogal R.M. Developmental exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin alters postnatal T cell phenotypes and T cell function and exacerbates autoimmune lupus in 24-week-old SNF1 mice. Birth Defects Res. A: Clin. Mol. Teratol. 2009, 85:828-836.
65. Nagayama J., Tsuji H., Iida T., Nakagawa R., Matsueda T., Hirakawa H., Yanagawa T., Fukushige J., Watanabe T. Immunologic effects of perinatal exposure to dioxins, PCBs and organochlorine pesticides in Japanese infants. Chemosphere 2007, 67:S393-S398.
66. Neubert R., Jacob-Muller U., Stahlmann R., Helge H., Neubert D. Polyhalogenated dibenzo-p-dioxins and dibenzofurans and the immune system. 1. Effects on peripheral lymphocyte subpopulations of a non-human primate (Callithrix jacchus) after treatment with 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Arch. Toxicol. 1990, 64:345-359.
67. Okuyama R., Abo T., Seki S., Ohteki T., Sugiura K., Kusumi A., Kumagai K. Estrogen administration activates extrathymic T cell differentiation in the liver. J. Exp. Med. 1992, 175:661-669.
68. Oughton J.A., Pereira C.B., DeKrey G.K., Collier J.M., Frank A.A., Kerkvliet N.I. Phenotypic analysis of spleen, thymus, and peripheral blood cells in aged C57B1/6 mice following long-term exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fundam. Appl. Toxicol. 1995, 25:60-69.
69. Padovan M., Govoni M., Castellino G., Rizzo N., Fotinidi M., Trotta F. Late onset systemic lupus erythematosus: no substantial differences using different cut-off ages. Rheumatol. Int. 2007, 27:735-741.
70. Palmer E. Negative selection-clearing out the bad apples from the T-cell repertoire. Nat. Rev. Immunol. 2003, 3:383-391.
71. Park Y.B., Lee S.K., Kim D.S., Lee J., Lee C.H., Song C.H. Elevated interleukin-10 levels correlated with disease activity in systemic lupus erythematosus. Clin. Exp. Rheumatol. 1998, 16:283-288.
72. Pietschmann P., Gollob E., Brosch S., Hahn P., Kudlacek S., Willheim M., Woloszczuk W., Peterlik M., Tragl K.H. The effect of age and gender on cytokine production by human peripheral blood mononuclear cells and markers of bone metabolism. Exp. Gerontol. 2003, 38:1119-1127.
73. Prelog M. Aging of the immune system: a risk factor for autoimmunity?. Autoimmun. Rev. 2006, 5:136-139.
74. Pu S.J., Luo S.F., Wu Y.J., Cheng H.S., Ho H.H. The clinical features and prognosis of lupus with disease onset at age 65 and older. Lupus 2000, 9:96-100.
75. Rocha B., Vassalli P., Guy-Grand D. The extrathymic T-cell development pathway. Immunol. Today 1992, 13:449-454.
76. Sandel P.C., Monroe J.G. Negative selection of immature B cells by receptor editing or deletion is determined by site of antigen encounter. Immunity 1999, 10:289-299.
77. Sebzda E., Mariathasan S., Ohteki T., Jones R., Bachmann M.F., Ohashi P.S. Selection of the T cell repertoire. Annu. Rev. Immunol. 1999, 17:829-874.
78. Souvannavong V., Lemaire C., Andreau K., Brown S., Adam A. Age-associated modulation of apoptosis and activation in murine B lymphocytes. Mech. Ageing Dev. 1998, 103:285-299.
79. Stacy S., Krolick K.A., Infante A.J., Kraig E. Immunological memory and late onset autoimmunity. Mech. Ageing Dev. 2002, 123:975-985.
80. Tarkowski M., Kur B., Nocun M., Sitarek K. Perinatal exposure of mice to TCDD decreases allergic sensitisation through inhibition of IL-4 production rather than T regulatory cell-mediated suppression. Int. J. Occup. Med. Environ. Health 2010, 23:75-83.
81. Tian Y., Ke S., Denison M.S., Rabson A.B., Gallo M.A. Ah receptor and NF-kappaB interactions, a potential mechanism for dioxin toxicity. J. Biol. Chem. 1999, 274:510-515.
82. Van der Put E., Sherwood E.M., Blomberg B.B., Riley R.L. Aged mice exhibit distinct B cell precursor phenotypes differing in activation, proliferation and apoptosis. Exp. Gerontol. 2003, 38:1137-1147.
83. Vorderstrasse B.A., Cundiff J.A., Lawrence B.P. A dose-response study of the effects of prenatal and lactational exposure to TCDD on the immune response to influenza a virus. J. Toxicol. Environ. Health A 2006, 69:445-463.
84. Voulgari P.V., Katsimbri P., Alamanos Y., Drosos A.A. Gender and age differences in systemic lupus erythematosus. A study of 489 Greek patients with a review of the literature. Lupus 2002, 11:722-729.
85. Weber H., Birnbaum L.S. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) and 2,3,7,8-tetrachlorodibenzofuran (TCDF) in pregnant C57BL/6N mice: distribution to the embryo and excretion. Arch. Toxicol. 1985, 57:159-162.
86. Weber H., Harris M.W., Haseman J.K., Birnbaum L.S. Teratogenic potency of TCDD, TCDF and TCDD-TCDF combinations in C57BL/6N mice. Toxicol. Lett. 1985, 26:159-167.
87. Weksler M.E., Szabo P. The effect of age on the B-cell repertoire. J. Clin. Immunol. 2000, 20:240-249.
88. Wyman A., Lavin A.L., Wilding G.E., Gasiewicz T.A. 2,3,7,8-Tetrachlorodibenzo-p-dioxin does not directly alter the phenotype of maturing B cells in a murine coculture system. Toxicol. Appl. Pharmacol. 2002, 180:164-177.
89. Yang X., Stedra J., Cerny J. Relative contribution of T and B cells to hypermutation and selection of the antibody repertoire in germinal centers of aged mice. J. Exp. Med. 1996, 183:959-970.
90. Zharhary D., Klinman N.R. Antigen responsiveness of the mature and generative B cell populations of aged mice. J. Exp. Med. 1983, 157:1300-1308.
91. Zheng B., Han S., Takahashi Y., Kelsoe G. Immunosenescence and germinal center reaction. Immunol. Rev. 1997, 160:63-77.