Circadian clock disruption in the mouse ovary in response to 2,3,7,8-tetrachlorodibenzo-p-dioxin

Toxicology Letters

Volumn 201, Issue 2, 2011, Pages 116-122

  Tischkau, Shelley A ^a   Jaeger, Cassie D ^a   Krager, Stacey L ^a  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AhR; BMAL1; Circadian rhythm; Ovary; PER2

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; PER2 PROTEIN; PROTEIN BMAL1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CIRCADIAN RHYTHM SLEEP DISORDER; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALS; ARNTL TRANSCRIPTION FACTORS; CIRCADIAN CLOCKS; FEMALE; MICE; MICE, INBRED C57BL; OVARY; PERIOD CIRCADIAN PROTEINS; RECEPTORS, ARYL HYDROCARBON; TETRACHLORODIBENZODIOXIN;

ANIMALIA; MUS;

EID: 79651475054     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2010.12.013     Document Type: Article

References (46)

1. Aylward L.L., Brunet R.C., Carrier G., Hays S.M., Cushing C.A., Needham L.L., Patterson D.G., Gerthoux P.M., Brambilla P., Mocarelli P. Concentration-dependent TCDD elimination kinetics in humans: toxicokinetic modeling for moderately to highly exposed adults from Seveso, Italy, and Vienna, Austria, and impact on dose estimates for the NIOSH cohort. J. Expo. Anal. Environ. Epidemiol. 2005, 15:51-65.
2. 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. Eukar. Gene Express. 2008, 18:207-250.
3. Birnbaum L.S. The mechanism of dioxin toxicity: relationship to risk assessment. Environ. Health Perspect. 1994, 102(Suppl. 9):157-167.
4. Borgs L., Beukelaers P., Vandenbosch R., Belachew S., Nguyen L., Malgrange B. Cell "circadian" cycle: new role for mammalian core clock genes. Cell Cycle 2009, 8:832-837.
5. Denison M.S., Fisher J.M., Whitlock J.P. Protein-DNA interactions at recognition sites for the dioxin-Ah receptor complex. J. Biol. Chem. 1989, 264:16478-16482.
6. Enan E., Matsumura F. Evidence for a second pathway in the action mechanism of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Significance of Ah-receptor mediated activation of protein kinase under cell-free conditions. Biochem. Pharmacol. 1995, 49:249-261.
7. Fahrenkrug J., Georg B., Hannibal J., Hindersson P., Gras S. Diurnal rhythmicity of the clock genes Per1 and Per2 in the rat ovary. Endocrinology 2006, 147:3769-3776.
8. Frame L., Li W., Miller J., Dickerson R. A proposed role for the arylhydrocarbon receptor (AhR) in non-photic feedback to the master circadian clock. Toxicologist 2004, 78:954.
9. Garrett R.W., Gasiewicz T.A. The aryl hydrocarbon receptor agonist 2,3,7,8-tetrachlorodibenzo-p-dioxin alters the circadian rhythms, quiescence, and expression of clock genes in murine hematopoietic stem and progenitor cells. Mol. Pharmacol. 2006, 69:2076-2083.
10. He P.J., Hirata M., Yamauchi N., Hashimoto S., Hattori M.A. The disruption of circadian clockwork in differentiating cells from rat reproductive tissues as identified by in vitro real-time monitoring system. J. Endocrinol. 2007, 193:413-420.
11. He P.J., Hirata M., Yamauchi N., Hashimoto S., Hattori M.A. Gonadotropic regulation of circadian clockwork in rat granulosa cells. Mol. Cell. Biochem. 2007, 302:111-118.
12. Hernandez-Ochoa I., Karman B.N., Flaws J.A. The role of the aryl hydrocarbon receptor in the female reproductive system. Biochem. Pharmacol. 2009, 77:547-559.
13. Hogenesch J.B., Chan W.K., Jackiw V.H., Brown R.C., Gu Y.-Z., Pray-Grant M., Perdew G.H., Bradfield C.A. Characterization of a subset of the basic-helix-loop-helix-PAS superfamily that interacts with components of the dioxin signaling pathway. J. Biol. Chem. 1997, 272:8581-8593.
14. Hogenesch J.B., Gu Y.Z., Jain S., Bradfield C.A. The basic-helix-loop-helix-PAS orphan MOP3 forms transcriptionally active complexes with circadian and hypoxia factors. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:5474-5479.
15. Huang P., Ceccatelli S., Rannug A. A study on diurnal mRNA expression of CYP1A1, AHR, ARNT and PER2 in rat pituitary and liver. Environ. Toxicol. Pharmacol. 2002, 11:119-126.
16. Karman B.N., Tischkau S.A. Circadian clock gene expression in the ovary: effects of luteinizing hormone. Biol. Reprod. 2006, 75:624-632.
17. Kleiner H.E., Vulimiri S.V., Hatten W.B., Reed M.J., Nebert D.W., Jefcoate C.R., DiGiovanni J. Role of cytochrome p4501 family members in the metabolic activation of polycyclic aromatic hydrocarbons in mouse epidermis. Chem. Res. Toxicol. 2004, 17:1667-1674.
18. Kulkarni P.S., Crespo J.G., Afonso C.A. Dioxins sources and current remediation technologies - a review. Environ. Int. 2008, 34:139-153.
19. Li X., Johnson D.C., Rozman K.K. Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on estrous cyclicity and ovulation in female Sprague-Dawley rats. Toxicol. Lett. 1995, 78:219-222.
20. Li X., Johnson D.C., Rozman K.K. Reproductive effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in female rats: ovulation, hormonal regulation, and possible mechanism(s). Toxicol. Appl. Pharmacol. 1995, 133:321-327.
21. McIntosh B.E., Hogenesch J.B., Bradfield C.A. Mammalian Per-Arnt-Sim proteins in environmental adaptation. Ann. Rev. Physiol. 2010, 72:625-645.
22. Miller J., Settachan D., Frame L., Dickerson R. 2,3,7,8-Tetrachlorodobenzo-p-dioxin phase advance the deer mouse (Peromyscus maniculatus) circadian rhythm by alterinf expression of clock proteins. Org. Comp. 1999, 42:23-28.
23. Miller K., Borgeest C., Greenfeld C., Tomic D., Flaws J. In utero effects of chemicals on reproductive tissues in females. Toxicol. Appl. Pharmacol. 2004, 198:111-131.
24. Mukai M., Lin T.M., Peterson R.E., Cooke P.S., Tischkau S.A. Behavioral rhythmicity of mice lacking AhR and attenuation of light-induced phase shift by 2,3,7,8-tetrachlorodibenzo-p-dioxin. J. Biol. Rhythm. 2008, 23:200-210.
25. Mukai M., Tischkau S.A. Effects of tryptophan photoproducts in the circadian timing system: searching for a physiological role for aryl hydrocarbon receptor. Toxicol. Sci. 2007, 95:172-181.
26. Nakamura T.J., Sellix M.T., Kudo T., Nakao N., Yoshimura T., Ebihara S., Colwell C.S., Block G.D. Influence of the estrous cycle on clock gene expression in reproductive tissues: effects of fluctuating ovarian steroid hormone levels. Steroids 2010, 75:203-212.
27. Nebert D.W., Dalton T.P., Okey A.B., Gonzalez F.J. Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J. Biol. Chem. 2004, 279:23847-23850.
28. Nebert D.W., Puga A., Vasiliou V. Role of the Ah receptor and the dioxin-inducible [Ah] gene battery in toxicity, cancer, and signal transduction. Ann. N. Y. Acad. Sci. 1993, 685:624-640.
29. Petroff B., Roby K., Gao X., Son D., Williams S., Johnson D., Rozman K., Terranova P. A review of mechanisms controlling ovulation with implications for the anovulatory effects of polychlorinated dibenzo-p-dioxins in rodents. Toxicology 2001, 158:91-107.
30. Petrulis J.R., Perdew G.H. The role of chaperone proteins in the aryl hydrocarbon receptor core complex. Chem. Biol. Interact. 2002, 141:25-40.
31. Pocar P., Fischer B., Klonisch T., Hombach-Klonisch S. Molecular interactions of the aryl hydrocarbon receptor and its biological and toxicological relevance for reproduction. Reproduction 2005, 129:379-389.
32. Pohjanvirta R., Unkila M., Tuomisto J. TCDD-induced hypophagia is not explained by nausea. Pharmacol. Biochem. Behav. 1994, 47:273-282.
33. Probst M.R., Fan C.M., Tessier-Lavigne M., Hankinson O. Two murine homologs of the Drosophila single-minded protein that interact with the mouse aryl hydrocarbon receptor nuclear translocator protein. J. Biol. Chem. 1997, 272:4451-4457.
34. Puga A., Hoffer A., Zhou S., Bohm J.M., Leikauf G.D., Shertzer H.G. Sustained increase in intracellular free calcium and activation of cyclooxygenase-2 expression in mouse hepatoma cells treated with dioxin. Biochem. Pharmacol. 1997, 54:1287-1296.
35. Puga A., Ma C., Marlowe J.L. The aryl hydrocarbon receptor cross-talks with multiple signal transduction pathways. Biochem. Pharmacol. 2009, 77:713-722.
36. Qu X., Metz R.P., Porter W.W., Cassone V.M., Earnest D.J. Disruption of clock gene expression alters responses of the aryl hydrocarbon receptor signaling pathway in the mouse mammary gland. Mol. Pharmacol. 2007, 72:1349-1358.
37. Qu X., Metz R.P., Porter W.W., Cassone V.M., Earnest D.J. Disruption of period gene expression alters the inductive effects of dioxin on the AhR signaling pathway in the mouse liver. Toxicol. Appl. Pharmacol. 2009, 234:370-377.
38. Qu X., Metz R.P., Porter W.W., Neuendorff N., Earnest B.J., Earnest D.J. The clock genes period 1 and period 2 mediate diurnal rhythms in dioxin-induced Cyp1A1 expression in the mouse mammary gland and liver. Toxicol. Lett. 2010, 196:28-32.
39. Ratajczak C.K., Boehle K.L., Muglia L.J. Impaired steroidogenesis and implantation failure in Bmal1-/- mice. Endocrinology 2009, 150:1879-1885.
40. Richardson V., Santostefano M., Birnbaum L.S. Daily cycle of bHLH-PAS proteins, Ah receptor and Arnt, in multiple tissues of female Sprague-Dawley rats. Biochem. Biophys. Res. Commun. 1998, 252:225-231.
41. Takahata S., Ozaki T., Mimura J., Kikuchi Y., Sogawa K., Fujii-Kuriyama Y. Transactivation mechanisms of mouse clock transcription factors, mClock and mArnt3. Genes Cells 2000, 5:739-747.
42. Tischkau, S., Howell, R., Hickok, J., Krager, S.L., Bahr, J.M., in press. The luteinizing hormone surge regulates circadian clock gene expression in the chicken ovary. Chronobiol. Int.
43. Tischkau S.A., Mitchell J.W., Tyan S.H., Buchanan G.F., Gillette M.U. Ca2+/cAMP response element-binding protein (CREB)-dependent activation of Per1 is required for light-induced signaling in the suprachiasmatic nucleus circadian clock. J. Biol. Chem. 2003, 278:718-723.
44. Travis C.C., Hattemer-Frey H.A. Human exposure to dioxin. Sci. Total Environ. 1991, 104:97-127.
45. Xu C.X., Krager S.L., Liao D.F., Tischkau S.A. Disruption of CLOCK-BMAL1 transcriptional activity is responsible for aryl hydrocarbon receptor-mediated regulation of Period1 gene. Toxicol. Sci. 2010, 115:98-108.
46. Yu W., Ikeda M., Abe H., Honma S., Ebisawa T., Yamauchi T., Honma K., Nomura M. Characterization of three splice variants and genomic organization of the mouse BMAL1 gene. Biochem. Biophys. Res. Commun. 1999, 260:760-767.