Unexpected gender difference in sensitivity to the acute toxicity of dioxin in mice

Toxicology and Applied Pharmacology

Volumn 262, Issue 2, 2012, Pages 167-176

  Pohjanvirta, Raimo ^a   Miettinen, Hanna ^b   Sankari, Satu ^a   Hegde, Nagabhooshan ^a   Lindén, Jere ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

2,3,7,8 tetrachlorodibenzo p dioxin; Acute toxicity; AH receptor; Gender differences; Sex hormones; TCDD

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; ANDROGEN; AROMATIC HYDROCARBON RECEPTOR; ESTROGEN; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; FEMALE; GONADECTOMY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY; PROTEIN EXPRESSION; SEX DIFFERENCE; TESTIS; WILD TYPE;

ANDROGENS; ANIMALS; ESTROGENS; FEMALE; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, TRANSGENIC; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ARYL HYDROCARBON; RNA, MESSENGER; SEX FACTORS; STATISTICS, NONPARAMETRIC; TETRACHLORODIBENZODIOXIN;

MUS; MUS MUSCULUS; RATTUS; RODENTIA;

EID: 84862248128     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2012.04.032     Document Type: Article

References (70)

1. Anonymous IFCC 1983/4: IFCC methods for the measurement of catalytic concentration of enzymes, part 5. IFCC method for alkaline phosphatase (orthophosphoric-monoesterphosphohydrolase, alkaline optimum, EC 3.1.3.1). J. Clin. Chem. Clin. Biochem. 1983, 21:731-748.
2. Anonymous IFCC 2002/5: IFCC primary reference procedures for the measurement of catalytic activity concentrations of enzymes at 37°C part 4. Reference procedure for the measurement of catalytic concentration of alanine aminotransferase. Clin. Chem. Lab. Med. 2002, 40:718-724.
3. Anonymous IFCC 2002/6: IFCC primary reference procedures for the measurement of catalytic activity concentrations of enzymes at 37°C part 5. Reference procedure for the measurement of catalytic concentration of aspartate aminotransferase. Clin. Chem. Lab. Med. 2002, 40:725-733.
4. Beatty P.W., Vaughn W.K., Neal R.A. Effect of alteration of rat hepatic mixed-function oxidase (MFO) activity on the toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicol. Appl. Pharmacol. 1978, 45:513-519.
5. Beischlag T.V., Luis Morales J., Hollingshead B.D., Perdew G.H. The aryl hydrocarbon receptor complex and the control of gene expression. Crit. Rev. Eukaryot. Gene Expr. 2008, 18:207-250.
6. Birnbaum L.S., McDonald M.M., Blair P.C., Clark A.M., Harris M.W. Differential toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in C57BL/6J mice congenic at the Ah Locus. Fundam. Appl. Toxicol. 1990, 15:186-200.
7. Bustin S.A. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol. 2000, 25:169-193.
8. Bustin S.A. Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): trends and problems. J. Mol. Endocrinol. 2002, 29:23-39.
9. Chapman D.E., Schiller C.M. Dose-related effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in C57BL/6J and DBA/2J mice. Toxicol. Appl. Pharmacol. 1985, 78:147-157.
10. Chubb C., Desjardins C. Steroid secretion by mouse testes perfused in vitro. Am. J. Physiol. 1983, 244:E575-E580.
11. Cohen A.N., Kapitulnik J., Ostrow J.D., Webster C.C. Effect of combined treatment with 2,3,7,8-tetrachlorodibenzo-p-dioxin and phototherapy on bilirubin metabolism in the jaundiced Gunn rat. Hepatology 1986, 6:490-494.
12. Commins S.P., Borish L., Steinke J.W. Immunologic messenger molecules: cytokines, interferons, and chemokines. J. Allergy Clin. Immunol. 2010, 125:S53-S72.
13. Couture-Haws L., Harris M.W., McDonald M.M., Lockhart A.C., Birnbaum L.S. Hydronephrosis in mice exposed to TCDD-contaminated breast milk: identification of the peak period of sensitivity and assessment of potential recovery. Toxicol. Appl. Pharmacol. 1991, 107:413-428.
14. Davarinos N.A., Pollenz R.S. Aryl hydrocarbon receptor imported into the nucleus following ligand binding is rapidly degraded via the cytosplasmic proteasome following nuclear export. J. Biol. Chem. 1999, 274:28708-28715.
15. Drucker C., Gewiese J., Malchow S., Scheller J., Rose-John S. Impact of interleukin-6 classic- and trans-signaling on liver damage and regeneration. J. Autoimmun. 2010, 34:29-37.
16. Enan E., El-Sabeawy F., Overstreet J., Matsumura F., Lasley B. Mechanisms of gender-specific TCDD-induced toxicity in guinea pig adipose tissue. Reprod. Toxicol. 1998, 12:357-369.
17. Franc M.A., Pohjanvirta R., Tuomisto J., Okey A.B. In vivo up-regulation of aryl hydrocarbon receptor expression by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in a dioxin-resistant rat model. Biochem. Pharmacol. 2001, 62:1565-1578.
18. Giannone J.V., Li W., Probst M., Okey A.B. Prolonged depletion of AH receptor without alteration of receptor mRNA levels after treatment of cells in culture with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Biochem. Pharmacol. 1998, 55:489-497.
19. Greig J.B., Francis J.E., Kay S.J., Lovell D.P., Smith A.G. Incomplete correlation of 2,3,7,8-tetrachlorodibenzo-p-dioxin hepatotoxicity with Ah phenotype in mice. Toxicol. Appl. Pharmacol. 1984, 74:17-25.
20. Greig J.B., Francis J.E., Kay S.J., Lister T., Ray D.E., Seawright A.A., Smith A.G. Pleiotropic effect of the gene hairless on hepatotoxicity of 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin in mice. Arch. Toxicol. 1987, 60:350-354.
21. Henck J.M., New M.A., Kociba R.J., Rao K.S. 2,3,7,8-Tetrachlorodibenzo-p-dioxin: acute oral toxicity in hamsters. Toxicol. Appl. Pharmacol. 1981, 59:405-407.
22. Hutchison J.B., Beyer C., Hutchison R.E., Wozniak A. Sex differences in the regulation of embryonic brain aromatase. J. Steroid Biochem. Mol. Biol. 1997, 61:315-322.
23. Jikumaru M., Hiramoto K., Honma T., Sato E.F., Sekiyama A., Inoue M. Effect of starvation on the survival of male and female mice. Physiol. Chem. Phys. Med. NMR 2007, 39:247-257.
24. Jones G., Greig J.B. Pathological changes in the liver of mice given 2,3,7,8-tetrachlorodibenzo-p-dioxin. Experientia 1975, 31:1315-1317.
25. Keller J.M., Huang J.C., Huet-Hudson Y., Leamy L.J. The effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on molar and mandible traits in congenic mice: a test of the role of the Ahr locus. Toxicology 2007, 242:52-62.
26. Kociba R.J., Keyes D.G., Beyer J.E., Carreon R.M., Wade C.E., Dittenber D.A., Kalnins R.P., Frauson L.E., Park C.N., Barnard S.D., Hummel R.A., Humiston C.G. Results of a two-year chronic toxicity and oncogenicity study of 2,3,7,8-tetrachlorodibenzo-p-dioxin in rats. Toxicol. Appl. Pharmacol. 1978, 46:279-303.
27. Kuil C.W., Brouwer A., van der Saag P.T., van der Burg B. Interference between progesterone and dioxin signal transduction pathways. Different mechanisms are involved in repression by the progesterone receptor A and B isoforms. J. Biol. Chem. 1998, 273:8829-8834.
28. Labrecque M.P., Takhar M.K., Hollingshead B.D., Prefontaine G.G., Perdew G.H., Beischlag T.V. Distinct roles for aryl hydrocarbon receptor nuclear translocator and ah receptor in estrogen-mediated signaling in human cancer cell lines. PLoS One 2012, 7:e29545.
29. Lucier G.W., McDaniel O.S., Hook G.E., Fowler B.A., Sonawane B.R., Faeder E. TCDD-induced changes in rat liver microsomal enzymes. Environ. Health Perspect. 1973, 5:199-209.
30. Ma Q. Overview of AHR functional domains and the classical AHR signaling pathway: induction of drug-metabolizing enzymes. The AH Receptor in Biology and Toxicology 2012, 35-45. John Wiley & Sons, Inc., Hoboken, NJ, USA. first edition. R. Pohjanvirta (Ed.).
31. Ma Q., Baldwin K.T. 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced degradation of aryl hydrocarbon receptor (AhR) by the ubiquitin-proteasome pathway. Role of the transcription activation and DNA binding of AhR. J. Biol. Chem. 2000, 275:8432-8438.
32. Malloy H.T., Evelyn K.A. The determination of bilirubin with the photoelectric colorimeter. J. Biol. Chem. 1937, 119:481-490.
33. Matsumura F. Nongenomic route of action of TCDD: identity, characteristics, and toxicological significance. The AH Receptor in Biology and Toxicology 2012, 197-215. John Wiley & Sons, Inc., Hoboken, NJ, USA. first edition. R. Pohjanvirta (Ed.).
34. Mayes J.S., Watson G.H. Direct effects of sex steroid hormones on adipose tissues and obesity. Obes. Rev. 2004, 5:197-216.
35. McConnell E.E., Moore J.A., Haseman J.K., Harris M.W. The comparative toxicity of chlorinated dibenzo-p-dioxins in mice and guinea pigs. Toxicol. Appl. Pharmacol. 1978, 44:335-356.
36. Neal R.A., Olson J.R., Gasiewicz T.A., Geiger L.E. The toxicokinetics of 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin in mammalian systems. Drug Metab. Rev. 1982, 13:355-385.
37. Niittynen, M., Simanainen, U., Pohjanvirta, R., Sankari, S., Tuomisto, J.T., submitted for publication. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) increases bilirubin formation but hampers quantitative hepatic conversion of biliverdin to bilirubin in rats with wild-type AH receptor.
38. Niu Y., Liang S. Microsatellite variation within three populations of inbred C57BL/6J strain. Zool. Res. 2008, 29:599-602.
39. Nukaya M., Moran S., Bradfield C.A. The role of the dioxin-responsive element cluster between the Cyp1a1 and Cyp1a2 loci in aryl hydrocarbon receptor biology. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:4923-4928.
40. Okey A.B. An aryl hydrocarbon receptor odyssey to the shores of toxicology: the Deichmann Lecture, International Congress of Toxicology-XI. Toxicol. Sci. 2007, 98:5-38.
41. Patel R.D., Murray I.A., Flaveny C.A., Kusnadi A., Perdew G.H. Ah receptor represses acute-phase response gene expression without binding to its cognate response element. Lab. Invest. 2009, 89:695-707.
42. Perkins L.M., Payne A.H. Quantification of P450scc, P450(17) alpha, and iron sulfur protein reductase in Leydig cells and adrenals of inbred strains of mice. Endocrinology 1988, 123:2675-2682.
43. Pohjanvirta R. Transgenic mouse lines expressing rat AH receptor variants - a new animal model for research on AH receptor function and dioxin toxicity mechanisms. Toxicol. Appl. Pharmacol. 2009, 236:166-182.
44. Pohjanvirta R., Tuomisto J. Short-term toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in laboratory animals: effects, mechanisms, and animal models. Pharmacol. Rev. 1994, 46:483-549.
45. Pohjanvirta R., Unkila M., Tuomisto J. Comparative acute lethality of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), 1,2,3,7,8-pentachlorodibenzo-p-dioxin and 1,2,3,4,7,8-hexachlorodibenzo-p-dioxin in the most TCDD-susceptible and the most TCDD-resistant rat strain. Pharmacol. Toxicol. 1993, 73:52-56.
46. Pohjanvirta R., Wong J.M., Li W., Harper P.A., Tuomisto J., Okey A.B. Point mutation in intron sequence causes altered carboxyl-terminal structure in the aryl hydrocarbon receptor of the most 2,3,7,8-tetrachlorodibenzo-p-dioxin-resistant rat strain. Mol. Pharmacol. 1998, 54:86-93.
47. Pohjanvirta R., Niittynen M., Linden J., Boutros P.C., Moffat I.D., Okey A.B. Evaluation of various housekeeping genes for their applicability for normalization of mRNA expression in dioxin-treated rats. Chem. Biol. Interact. 2006, 160:134-149.
48. Pohjanvirta R., Korkalainen M., Moffat I.D., Boutros P.C., Okey A.B. Role of the AHR and its structure in TCDD toxicity. The AH Receptor in Biology and Toxicology 2012, 181-196. John Wiley & Sons, Inc., Hoboken, NJ, USA. first edition. R. Pohjanvirta (Ed.).
49. Poland A., Palen D., Glover E. Analysis of the four alleles of the murine aryl hydrocarbon receptor. Mol. Pharmacol. 1994, 46:915-921.
50. Pollenz R.S. The aryl-hydrocarbon receptor, but not the aryl-hydrocarbon receptor nuclear translocator protein, is rapidly depleted in hepatic and nonhepatic culture cells exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Mol. Pharmacol. 1996, 49:391-398.
51. Pollenz R.S., Santostefano M.J., Klett E., Richardson V.M., Necela B., Birnbaum L.S. Female Sprague-Dawley rats exposed to a single oral dose of 2,3,7,8-tetrachlorodibenzo-p-dioxin exhibit sustained depletion of aryl hydrocarbon receptor protein in liver, spleen, thymus, and lung. Toxicol. Sci. 1998, 42:117-128.
52. 50 values from the method of Miller and Tainter, 1944. J. Ayub Med. Coll. Abbottabad 2009, 21:184-185.
53. Sanada N., Gotoh Y., Shimazawa R., Klinge C.M., Kizu R. Repression of activated aryl hydrocarbon receptor-induced transcriptional activation by 5alpha-dihydrotestosterone in human prostate cancer LNCaP and human breast cancer T47D cells. J. Pharmacol. Sci. 2009, 109:380-387.
54. Schwetz B.A., Norris J.M., Sparschu G.L., Rowe U.K., Gehring P.J., Emerson J.L., Gerbig C.G. Toxicology of chlorinated dibenzo-p-dioxins. Environ. Health Perspect. 1973, 5:87-99.
55. Scotland R.S., Stables M.J., Madalli S., Watson P., Gilroy D.W. Sex differences in resident immune cell phenotype underlie more efficient acute inflammatory responses in female mice. Blood 2011, 118:5918-5927.
56. Straub R.H. The complex role of estrogens in inflammation. Endocr. Rev. 2007, 28:521-574.
57. Tanos R., Patel R.D., Murray I.A., Smith P.B., Patterson A.D., Perdew G.H. Ah receptor regulates the cholesterol biosynthetic pathway in a dioxin response element-independent manner. Hepatology 2012, (Electronic publication ahead of print). doi:10.1002/hep.25571.
58. Trinder P. Determination of glucose in blood using glucose oxidase with an alternative oxygen acceptor. Ann. Clin. Biochem. 1969, 6:24-27.
59. Tuomisto J.T., Viluksela M., Pohjanvirta R., Tuomisto J. The AH receptor and a novel gene determine acute toxic responses to TCDD: segregation of the resistant alleles to different rat lines. Toxicol. Appl. Pharmacol. 1999, 155:71-81.
60. Ueyama T., Shirasawa N., Numazawa M., Yamada K., Shelangouski M., Ito T., Tsuruo Y. Gastric parietal cells: potent endocrine role in secreting estrogen as a possible regulator of gastro-hepatic axis. Endocrinology 2002, 143:3162-3170.
61. Unkila M., Pohjanvirta R., MacDonald E., Tuomisto J.T., Tuomisto J. Dose response and time course of alterations in tryptophan metabolism by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in the most TCDD-susceptible and the most TCDD-resistant rat strain: relationship with TCDD lethality. Toxicol. Appl. Pharmacol. 1994, 128:280-292.
62. Uno S., Dalton T.P., Sinclair P.R., Gorman N., Wang B., Smith A.G., Miller M.L., Shertzer H.G., Nebert D.W. Cyp1a1(-/-) male mice: protection against high-dose TCDD-induced lethality and wasting syndrome, and resistance to intrahepatocyte lipid accumulation and uroporphyria. Toxicol. Appl. Pharmacol. 2004, 196:410-421.
63. Vanderschueren D., Gaytant J., Boonen S., Venken K. Androgens and bone. Curr. Opin. Endocrinol. Diabetes Obes. 2008, 15:250-254.
64. Vos J.G., Moore J.A., Zinkl J.G. Toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in C57B1/6 mice. Toxicol. Appl. Pharmacol. 1974, 29:229-241.
65. Wahlefeld A.W. Triglycerides. Determination after enzymatic hydrolysis. Methods of Enzymatic Analysis 1974, vol. 4:1831-1835. Academic Press, New York. second English edition. H.U. Bergmeyer (Ed.).
66. Walker N.J., Gastel J.A., Costa L.T., Clark G.C., Lucier G.W., Sutter T.R. Rat CYP1B1: an adrenal cytochrome P450 that exhibits sex-dependent expression in livers and kidneys of TCDD-treated animals. Carcinogenesis 1995, 16:1319-1327.
67. Watkins-Chow D.E., Pavan W.J. Genomic copy number and expression variation within the C57BL/6J inbred mouse strain. Genome Res. 2008, 18:60-66.
68. Weber L.W., Lebofsky M., Stahl B.U., Smith S., Rozman K.K. Correlation between toxicity and effects on intermediary metabolism in 2,3,7,8-tetrachlorodibenzo-p-dioxin-treated male C57BL/6J and DBA/2J mice. Toxicol. Appl. Pharmacol. 1995, 131:155-162.
69. Wihlen B., Ahmed S., Inzunza J., Matthews J. Estrogen receptor subtype- and promoter-specific modulation of aryl hydrocarbon receptor-dependent transcription. Mol. Cancer Res. 2009, 7:977-986.
70. Zhu B.T., Gallo M.A., Burger C.W., Meeker R.J., Cai M.X., Xu S., Conney A.H. Effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin administration and high-fat diet on the body weight and hepatic estrogen metabolism in female C3H/HeN mice. Toxicol. Appl. Pharmacol. 2008, 226:107-118.