The systemic and gonadal toxicity of 3-methylcholanthrene is prevented by daily administration of α-naphthoflavone

Toxicology

Volumn 353-354, Issue , 2016, Pages 58-69

  Rhon Calderón, Eric Alejandro ^a   Galarza, Rocío Alejandra ^a   Lomniczi, Alejandro ^b   Faletti, Alicia Graciela ^a  

^a Centre de Estudios Farmacologicos y Botanicos   (Argentina)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

3 Methylcholanthrene; Follicular growth; Ovulation; Naphthoflavone

Indexed keywords

3 METHYLCHOLANTHRENE; ALPHA NAPHTHOFLAVONE; AROMATIC HYDROCARBON RECEPTOR; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; MESSENGER RNA; ALPHA-NAPHTHOFLAVONE; BENZOFLAVONE DERIVATIVE; CYP1B1 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BONE MARROW CELL; CONCENTRATION RESPONSE; CONTROLLED STUDY; ESTRUS CYCLE; FEMALE; GENE OVEREXPRESSION; GENETIC DAMAGE; NONHUMAN; OOCYTE; ORGAN WEIGHT; OVARIAN RESERVE; OVARIAN WEIGHT; OVARY FOLLICLE; OVARY FUNCTION; OVULATION; PRIORITY JOURNAL; RAT; REPRODUCTIVE TOXICITY; SEXUAL MATURITY; WEIGHT GAIN; ANIMAL; CHROMATIN IMMUNOPRECIPITATION; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; BENZOFLAVONES; BONE MARROW CELLS; CHROMATIN IMMUNOPRECIPITATION; CYTOCHROME P-450 CYP1A1; CYTOCHROME P-450 CYP1B1; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GENE EXPRESSION REGULATION; METHYLCHOLANTHRENE; OOCYTES; OVARIAN FOLLICLE; OVULATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ARYL HYDROCARBON;

EID: 84968880027     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2016.05.005     Document Type: Article

References (66)

1. Aluru N., Renaud R., Leatherland J.F., Vijayan M.M. Ah Receptor-mediated impairment of interrenal steroidogenesis involves StAR protein and P450scc gene attenuation in rainbow trout. Toxicol. Sci. 2005, 84:260-269.
2. Barnett K.R., Tomic D., Gupta R.K., Miller K.P., Meachum S., Paulose T., Flaws J.A. The aryl hydrocarbon receptor affects mouse ovarian follicle growth via mechanisms involving estradiol regulation and responsiveness. Biol. Reprod. 2007, 76:1062-1070.
3. Barnett K.R., Tomic D., Gupta R.K., Babus J.K., Roby K.F., Terranova P.F., Flaws J.A. The aryl hydrocarbon receptor is required for normal gonadotropin responsiveness in the mouse ovary. Toxicol. Appl. Pharmacol. 2007, 223:66-72.
4. Barreiro K.A., Di Yorio M.P., Artillo-Guida R.D., Paz D.A., Faletti A.G. Daily treatment with α-naphthoflavone enhances follicular growth and ovulation rate in the rat. Toxicol. Appl. Pharmacol. 2011, 252:11-17.
5. Benedict J.C., Lin T.M., Loeffler I.K., Peterson R.E., Flaws J.A. Physiological role of the aryl hydrocarbon receptor in mouse ovary development. Toxicol. Sci. 2000, 56:382-388.
6. Benedict J.C., Miller K.P., Lin T.M., Greenfeld C., Babus J.K., Peterson R.E., Flaws J.A. Aryl hydrocarbon receptor regulates growth but not atresia, of mouse preantral and antral follicles. Biol. Reprod. 2003, 68:1511-1517.
7. Berthelot-Ricou A., Perrin J., di Giorgio C., de Meo M., Botta A., Courbiere B. Assessment of 1,2-propanediol (PrOH) genotoxicity on mouse oocytes by comet assay. Fertil. Steril. 2011, 96:1002-1007.
8. Boffetta P., Jourenkova N., Gustavsson P. Cancer risk from occupational and environmental exposure to polycyclic aromatic hydrocarbons. Cancer Causes Control 1997, 8:444-472.
9. Borman S.M., Christian P.J., Sipes I.G., Hoyer P.B. Ovotoxicity in female Fischer rats and B6 mice induced by low-dose exposure to three polycyclic aromatic hydrocarbons: comparison through calculation of an ovotoxic index. Toxicol. Appl. Pharmacol. 2000, 167:191-198.
10. Cavalieri E., Roth R., Althoff J., Grandjean C., Patil K., Marsh S., Mclaughlin D. Carcinogenicity and metabolic profiles of 3-methylcholanthrene oxygenated derivatives at the 1 and 2 positions. Chem. Biol. Interact. 1978, 22:69-81.
11. Cebral E., Abrevaya X.C., Mudry M.D. Male and female reproductive toxicity induced by sub-chronic ethanol exposure in CF-1 mice. Cell Biol. Toxicol. 2011, 27:237-248.
12. Chaffin C.L., Trewin A.L., Hutz R.J. Estrous cycle-dependent changes in the expression of aromatic hydrocarbon receptor (AHR) and AHR-nuclear translocator (ARNT) mRNAs in the rat ovary and liver. Chem. Biol. Interact. 2000, 124:205-216.
13. Chahin A., Peiffer J., Olry J.C., Crepeaux G., Schroeder H., Rychen G., Guiavarc'h Y. EROD activity induction in peripheral blood lymphocytes: liver and brain tissues of rats orally exposed to polycyclic aromatic hydrocarbons. Food Chem. Toxicol. 2013, 56:371-380.
14. Chang T.K., Gonzalez F.J., Waxman D.J. Evaluation of triacetyloleandomycin: alpha-naphthoflavone and diethyldithiocarbamate as selective chemical probes for inhibition of human cytochromes P450. Arch. Biochem. Biophys. 1994, 311:437-442.
15. Conney A.H. Induction of microsomal enzymes by foreign chemicals and carcinogenesis by polycyclic aromatic hydrocarbons: G H. A. Clowes Memorial Lecture. Cancer Res. 1982, 42:4875-4917.
16. Davis B.J., Mccurdy E.A., Miller B.D., Lucier G.W., Tritscher A.M. Ovarian tumors in rats induced by chronic 2,3,7,8-tetrachlorodibenzo-p-dioxin treatment. Cancer Res. 2000, 60:5414-5419.
17. Einaudi L., Courbiere B., Tassistro V., Prevot C., Sari-Minodier I., Orsiere T., Perrin J. In vivo exposure to benzo(a)pyrene induces significant DNA damage in mouse oocytes and cumulus cells. Hum. Reprod. 2014, 29:548-554.
18. Faletti A.G., Viggiano J.M., Gimeno M.A. Beta-endorphin inhibits prostaglandin synthesis in rat ovaries and blocks induced ovulation. Prostaglandins 1995, 49:93-103.
19. Fieser L.F., Fieser M. Natural Products Related to Phenanthrene 1949, Rheinhold Publishing Corporation, New York. 3rd ed.
20. Flesher J.W., Horn J., Lehner A.F. Carcinogenicity of 1-hydroxy-3-methylcholanthrene and its electrophilic sulfate ester 1-sulfooxy-3-methylcholanthrene in Sprague-Dawley rats. Biochem. Biophys. Res. Commun. 1998, 243:30-35.
21. Fujii-Kuriyama Y., Mimura J. Molecular mechanisms of AhR functions in the regulation of cytochrome P450 genes. Biochem. Biophys. Res. Commun. 2005, 338:311-317.
22. Fukuda I., Mukai R., Kawase M., Yoshida K., Ashida H. Interaction between the aryl hydrocarbon receptor and its antagonists: flavonoids. Biochem. Biophys. Res. Commun. 2007, 359:822-827.
23. Gasiewicz T.A., Rucci G. Alpha-naphthoflavone acts as an antagonist of 2,3,7,8-tetrachlorodibenzo-p-dioxin by forming an inactive complex with the Ah receptor. Mol. Pharmacol. 1991, 40:607-612.
24. Gasiewicz T.A., Kende A.S., Rucci G., Whitney B., Willey J.J. Analysis of structural requirements for Ah receptor antagonist activity: ellipticines flavones, and related compounds. Biochem. Pharmacol. 1996, 52:1787-1803.
25. Guengerich F.P., Shimada T. Activation of procarcinogens by human cytochrome P450 enzymes. Mutat. Res. 1998, 400:201-213.
26. Hahn M.E. Aryl hydrocarbon receptors: diversity and evolution. Chem. Biol. Interact. 2002, 141:131-160.
27. Hernández-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.
28. Hernández-Ochoa I., Barnett-Ringgold K.R., Dehlinger S.L., Gupta R.K., Leslie T.C., Roby K.F., Flaws J.A. The ability of the aryl hydrocarbon receptor to regulate ovarian follicle growth and estradiol biosynthesis in mice depends on stage of sexual maturity. Biol. Reprod. 2010, 83:698-706.
29. Khorram O., Garthwaite M., Golos T. Uterine and ovarian aryl hydrocarbon receptor (AHR) and aryl hydrocarbon receptor nuclear translocator (ARNT) mRNA expression in benign and malignant gynaecological conditions. Mol. Hum. Reprod. 2002, 8:75-80.
30. Kondraganti S.R., Muthiah K., Jiang W., Barrios R., Moorthy B. Effects of 3-methylcholanthrene on gene expression profiling in the rat using cDNA microarray analyses. Chem. Res. Toxicol. 2005, 18:1634-1641.
31. Konstandi M., Pappas P., Johnson E., Lecklin A., Karageorgou M., Marselos M. Modification of reproductive function in the rat by 3-methylcholanthrene. Pharmacol. Res. 1997, 35:107-111.
32. Kröller E. Ergebnisse vergleichender Schwel- und Rauchversuche an Tabak. Dtsch Lebensm-Rundsch 1964, 60:214-215.
33. Lomniczi A., Loche A., Castellano J.M., Ronnekleiv O.K., Bosch M., Kaidar G., Knoll J.G., Wright H., Pfeifer G.P., Ojeda S.R. Epigenetic control of female puberty. Nat. Neurosci. 2013, 16:281-289.
34. Lomniczi A., Wright H., Castellano J.M., Matagne V., Toro C.A., Ramaswamy S., Plant T.M., Ojeda S.R. Epigenetic regulation of puberty via Zinc finger protein-mediated transcriptional repression. Nat. Commun. 2015, 6:10195.
35. Lu Y.F., Santostefano M., Cunningham B.D., Threadgill M.D., Safe S. Substituted flavones as aryl hydrocarbon (Ah) receptor agonists and antagonists. Biochem. Pharmacol. 1996, 51:1077-1087.
36. Mattison D.R., Thorgeirsson S.S. Gonadal aryl hydrocarbon hydroxylase in rats and mice. Cancer Res. 1978, 38:1368-1373.
37. Mattison D.R., Thorgeirsson S.S. Ovarian aryl hydrocarbon hydroxylase activity and primordial oocyte toxicity of polycyclic aromatic hydrocarbons in mice. Cancer Res. 1979, 39:3471-3475.
38. Mattison D.R. Morphology of oocyte and follicle destruction by polycyclic aromatic hydrocarbons in mice. Toxicol. Appl. Pharmacol. 1980, 53:249-259.
39. Meinl W., Tsoi C., Swedmark S., Tibbs Z.E., Falany C.N., Glatt H. Highly selective bioactivation of 1- and 2-hydroxy-3-methylcholanthrene to mutagens by individual human and other mammalian sulphotransferases expressed in Salmonella typhimurium. Mutagenesis 2013, 28:609-619.
40. Mense S.M., Singh B., Remotti F., Liu X., Bhat H.K. Vitamin C and alpha-naphthoflavone prevent estrogen-induced mammary tumors and decrease oxidative stress in female ACI rats. Carcinogenesis 2009, 30:1202-1208.
41. Miao W., Jin Y., Lin X., Fu Z. Differential expression of the main polycyclicaromatic hydrocarbon responsive genes in the extrahepatic tissues of mice. Environ. Toxicol. Pharmacol. 2014, 37:885-894.
42. Moorthy B., Miller K.P., Jiang W., Ramos K.S. The atherogen 3-methylcholanthrene induces multiple DNA adducts in mouse aortic smooth muscle cells: role of cytochrome P4501B1. Cardiovasc. Res. 2002, 53:1002-1009.
43. Murray I.A., Patterson A.D., Perdew G.H. Aryl hydrocarbon receptor ligands in cancer: friend and foe. Nat. Rev. Cancer 2014, 14:801-814.
44. Myers M., Britt K.L., Wreford N.G., Ebling F.J., Kerr J.B. Methods for quantifying follicular numbers within the mouse ovary. Reproduction 2004, 127:569-580.
45. Neal M.S., Zhu J., Holloway A.C., Foster W.G. Follicle growth is inhibited by benzo-[a]-pyrene at concentrations representative of human exposure, in an isolated rat follicle culture assay. Hum. Reprod. 2007, 22:961-967.
46. Neal M.S., Zhu J., Foster W.G. Quantification of benzo[a]pyrene and other PAHs in the serum and follicular fluid of smokers versus non-smokers. Reprod. Toxicol. 2008, 25:100-106.
47. Olive P.L., Banáth J.P. The comet assay: a method to measure DNA damage in individual cells. Nat. Protoc. 2006, 1:23-29.
48. Pansoy A., Ahmed S., Valen E., Sandelin A., Matthews J. 3-Methylcholanthrene induces differential recruitment of aryl hydrocarbon receptor to human promoters. Toxicol. Sci. 2010, 117:90-100.
49. Patel M.M., Bhat H.K. Differential oxidant potential of carcinogenic and weakly carcinogenic estrogens: involvement of metabolic activation and cytochrome P450. J. Biochem. Mol. Toxicol. 2004, 18:37-42.
50. Pleil J.D., Stiegel M.A., Sobus J.R., Tabucchi S., Ghio A.J., Madden M.C. Cumulative exposure assessment for trace-level polycyclic aromatic hydrocarbons (PAH) using human blood and plasma analysis. J. Chromatogr. B 2010, 878:1753-1760.
51. Pleil J.D., Stiegel M.A., Madden M.C., Sobus J.R. Heat map visualization of complex environmental and biomarker measurements. Chemosphere 2011, 84:716-723.
52. Robles R., Morita Y., Mann K.K., Perez G.I., Yang S., Matikainen T., Sherr D.H., Tilly J.L. The aryl hydrocarbon receptor, a basic helix-loop-helix transcription factor of the PAS gene family, is required for normal ovarian germ cell dynamics in the mouse. Endocrinology 2000, 141:450-453.
53. Rodgman A., Cook L.C. The composition of cigarette smoke. An historical perspective of several polycyclic aromatic hydrocarbons. Beitr. Tabakforsch. Int. 2009, 23:384-410.
54. Rodgman A., Perfetti T.A. The Chemical Components of Tobacco and Tobacco Smoke 2013, CRC Press Taylor & Francis Group, Boca Raton, Florida. second ed.
55. Schmid W. The micronucleus test. Mutat. Res. 1975, 31:9-15.
56. Shimada T., Sugie A., Shindo M., Nakajima T., Azuma E., Hashimoto M., Inoue K. Tissue-specific induction of cytochromes P450 1A1 and 1B1 by polycyclic aromatic hydrocarbons and polychlorinated biphenyls in engineered C57BL/6J mice of arylhydrocarbon receptor gene. Toxicol. Appl. Pharmacol. 2003, 187:1-10.
57. Shimada T. Xenobiotic-metabolizing enzymes involved in activation and detoxification of carcinogenic polycyclic aromatic hydrocarbons. Drug Metab. Pharmacokinet. 2006, 21:257-276.
58. Shiromizu K., Mattison D.R. Murine oocyte destruction following intraovarian treatment with 3-methylcholanthrene or 7,12-dimethylbenz(a)anthracene: protection by alpha-naphthoflavone. Teratog. Carcinog. Mutagen. 1985, 5:463-472.
59. Sims P. The carcinogenic activities in mice of compounds related to 3-methylcholanthrene. Int. J. Cancer 1967, 2:505-508.
60. Sims P. Qualitative and quantitative studies on the metabolism of a series of aromatic hydrocarbons by rat-liver preparations. Biochem. Pharmacol. 1970, 19:795-818.
61. Sinal C.J., Webb C.D., Bend J.R. Differential in vivo effects of alpha-naphthoflavone and beta-naphthoflavone on CYP1A1 and CYP2E1 in rat liver, lung, heart, and kidney. J. Biochem. Mol. Toxicol. 1999, 13:29-40.
62. Sobinoff A.P., Nixon B., Roman S.D., McLaughlin E.A. Staying alive: PI3K pathway promotes primordial follicle activation and survival in response to 3MC-induced ovotoxicity. Toxicol. Sci. 2012, 128:258-271.
63. Stewart B.W., Haski R. Relationships between carcinogen metabolism: adduct binding and DNA damage in 3-methylcholanthrene-exposed lung. Chem. Biol. Interact. 1984, 52:111-128.
64. Thompson K.E., Bourguet S.M., Christian P.J., Benedict J.C., Sipes I.G., Flaws J.A., Hoyer P.B. Differences between rats and mice in the involvement of the aryl hydrocarbon receptor in 4-vinylcyclohexene diepoxide-induced ovarian follicle loss. Toxicol. Appl. Pharmacol. 2005, 203:114-123.
65. Xu M., Nelson G.B., Moore J.E., McCoy T.P., Dai J., Manderville R.A., Ross J.A., Miller M.S. Induction of Cyp1a1 and Cyp1b1 and formation of DNA adducts in C57BL/6 Balb/c, and F1 mice following in utero exposure to 3-methylcholanthrene. Toxicol. Appl. Pharmacol. 2005, 209:28-38.
66. Zhang S., Qin C., Safe S.H. Flavonoids as aryl hydrocarbon receptor agonists/antagonists: effects of structure and cell context. Environ. Health Perspect. 2003, 111:1877-1882.