Adding insult to injury: Effects of xenobiotic-induced preantral ovotoxicity on ovarian development and oocyte fusibility

Toxicological Sciences

Volumn 118, Issue 2, 2010, Pages 653-666

  Sobinoff, Alexander P ^a   Pye, Victoria ^a   Nixon, Brett ^a   Roman, Shaun D ^a   McLaughlin, Eileen A ^a  

^a UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

Fertility; Oocyte dysfunction; Ovary; Primordial follicle; Xenobiotic

Indexed keywords

4 VINYLCYCLOHEXENE DIEPOXIDE; MENADIONE; METHOXYCHLOR; TRANSCRIPTOME; UNCLASSIFIED DRUG; XENOBIOTIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL DEATH; CELL FUSION; CONTROLLED STUDY; CYTOTOXICITY; FEMALE; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; IN VITRO STUDY; IN VIVO STUDY; LIPID PEROXIDATION; MALE; MICROARRAY ANALYSIS; MOUSE; NEWBORN; NONHUMAN; OOCYTE; OVARY DEVELOPMENT; OVARY FOLLICLE ATRESIA; OVARY FOLLICLE DEVELOPMENT; OVOTOXICITY; POLYMERASE CHAIN REACTION; SPERM;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; CYCLOHEXENES; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; LIPID PEROXIDATION; MALE; METHOXYCHLOR; MICE; MICROARRAY ANALYSIS; ORGAN CULTURE TECHNIQUES; OVARIAN FOLLICLE; OVUM; OXIDATIVE STRESS; RNA, MESSENGER; SPERM-OVUM INTERACTIONS; TISSUE ARRAY ANALYSIS; VINYL COMPOUNDS; VITAMIN K 3;

MAMMALIA; MUS;

EID: 78549282780     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq272     Document Type: Article

References (54)

1. Bayrak, A., and Oktay, K. (2003). The expression of cyclin-dependent kinase inhibitors p 15, p 16, p 21, and p 27 during ovarian follicle growth initiation in the mouse. Reprod. Biol. Endocrinol. 1, 41.
2. Borgeest, C., Miller, K.P., Gupta, R., Greenfeld, C., Hruska, K.S., Hoyer, P., and Flaws, J.A. (2004). Methoxychlor-induced atresia in the mouse involves Bcl-2 family members, but not gonadotropins or estradiol. Biol. Reprod. 70, 1828-1835.
3. Borgeest, C., Symonds, D., Mayer, L.P., Hoyer, P.B., and Flaws, J.A. (2002). Methoxychlor may cause ovarian follicular atresia and proliferation of the ovarian epithelium in the mouse. Toxicol. Sci. 68, 473-478.
4. Borman, S.M., Christian, P.J., Sipes, I.G., and Hoyer, P.B. (2000). 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. 167, 191-198.
5. Boyer, A., Goff, A.K., and Boerboom, D. (2009). WNT signaling in ovarian follicle biology and tumorigenesis. Trends Endocrinol. Metab. 21, 25-32.
6. Brown, C., LaRocca, J., Pietruska, J., Ota, M., Anderson, L., Duncan Smith, S., Weston, P., Rasoulpour, T., and Hixon, M.L. (2010). Subfertility caused by altered follicular development and oocyte growth in female mice lacking PKBalpha/Akt1. Biol. Reprod. 82, 246-256.
7. Cadenas, E., and Davies, K.J.A. (2000). Mitochondrial free radical generation, oxidative stress, and aging. Free Radic. Biol. Med. 29, 222-230.
8. Cannady, E.A., Dyer, C.A., Christian, P.J., Sipes, I.G., and Hoyer, P.B. (2003). Expression and activity of cytochromes P450 2E1, 2A, and 2B in the mouse ovary: the effect of 4-vinylcyclohexene and its diepoxide metabolite. Toxicol. Sci. 73, 423-430.
9. Chapman, D.L., and Wolgemuth, D.J. (1994). Expression of proliferating cell nuclear antigen in the mouse germ line and surrounding somatic cells suggests both proliferation-dependent and -independent modes of function. Int. J. Dev. Biol. 38, 491-497.
10. Chomczynski, P., and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform. Anal. Biochem. 162, 156-159.
11. Danielson, P.B. (2002). The cytochrome P450 superfamily: biochemistry, evolution and drug metabolism in humans. Curr. Drug Metab. 3, 561-597.
12. Datta, S.R., Brunet, A., and Greenberg, M.E. (1999). Cellular survival: a play in three Akts. Genes Dev. 13, 2905-2927.
13. Devine, P.J., Sipes, I.G., Skinner, M.K., and Hoyer, P.B. (2002). Characterization of a rat in vitro ovarian culture system to study the ovarian toxicant 4-vinylcyclohexene diepoxide. Toxicol. Appl. Pharmacol. 184, 107-115.
14. Diaz, F.J., Wigglesworth, K., and Eppig, J.J. (2007). Oocytes are required for the preantral granulosa cell to cumulus cell transition in mice. Dev. Biol. 305, 300-311.
15. Frade, R., Balbo, M., and Barel, M. (2002). RB18A regulates p53-dependent apoptosis. Oncogene 21, 861-866.
16. Gupta, R.K., Meachum, S., Hernández-Ochoa, I., Peretz, J., Yao, H.H., and Flaws, J.A. (2009). Methoxychlor inhibits growth of antral follicles by altering cell cycle regulators. Toxicol. Appl. Pharmacol. 240, 1-7.
17. Gupta, R.K., Schuh, R.A., Fiskum, G., and Flaws, J.A. (2006). Methoxychlor causes mitochondrial dysfunction and oxidative damage in the mouse ovary. Toxicol. Appl. Pharmacol. 216, 436-445.
18. Hirshfield, A.N. (1991). Development of follicles in the mammalian ovary. Int. Rev. Cytol. Surv. Cell Biol. 124, 43-101.
19. Holt, J.E., Jackson, A., Roman, S.D., Aitken, R.J., Koopman, P., and McLaughlin, E.A. (2006). CXCR4/SDF1 interaction inhibits the primordial to primary follicle transition in the neonatal mouse ovary. Dev. Biol. 293, 449-460.
20. Hoyer, P.B., and Sipes, I.G. (1996). Assessment of follicle destruction in chemical-induced ovarian toxicity. Annu. Rev. Pharmacol. Toxicol. 36, 307-331.
21. Hu, X., Christian, P., Sipes, I.G., and Hoyer, P.B. (2001). Expression and redistribution of cellular Bad, Bax, and Bcl-xL protein is associated with VCD-induced ovotoxicity in rats. Biol. Reprod. 65, 1489-1495.
22. Hu, X., Flaws, J.A., Sipes, I.G., and Hoyer, P.B. (2002). Activation of mitogen-activated protein kinases and AP-1 transcription factor in ovotoxicity induced by 4-vinylcyclohexene diepoxide in rats. Biol. Reprod. 67, 718-724.
23. Hu, X., Roberts, J.R., Apopa, P.L., Kan, Y.W., and Ma, Q. (2006). Accelerated ovarian failure induced by 4-vinyl cyclohexene diepoxide in Nrf2 null mice. Mol. Cell. Biol. 26, 940-954.
24. Huang, J.H.Y., Rajkovic, A., Szafranski, P., Ochsner, S., Richards, J.A., and Goode, S. (2003). Expression of Drosophila neoplastic tumor suppressor genes discslarge, scribble, and lethal giant larvae in the mammalian ovary. Gene Expr. Patterns. 3, 3-11.
25. Hutt, K.J., McLaughlin, E.A., and Holland, M.K. (2006). Primordial follicle activation and follicular development in the juvenile rabbit ovary. Cell Tissue Res. 326, 809-822.
26. Jarabak, R., and Jarabak, J. (1995). Effect of ascorbate on the DTdiaphorase-mediated redox cycling of 2-methyl-1, 4-naphthoquinone. Arch. Biochem. Biophys. 318, 418-423.
27. Kantengwa, S., Jornot, L., Devenoges, C., and Nicod, L.P. (2003). Superoxide anions induce the maturation of human dendritic cells. Am. J. Respir. Critic. Care Med. 167, 431-437.
28. Kao, S.W., Sipes, I.G., and Hoyer, P.B. (1999). Early effects of ovotoxicity induced by 4-vinylcyclohexene diepoxide in rats and mice. Reprod. Toxicol. 13, 67-75.
29. Kascheike, B., and Walther, N. (1997). Alterations in the chromatin structure of the distal promoter region of the bovine oxytocin gene correlate with ovarian expression. DNA Cell Biol. 16, 1237-1248.
30. Keating, A.F., Mark, C.J., Sen, N., Sipes, I.G., and Hoyer, P.B. (2009). Effect of phosphatidylinositol-3 kinase inhibition on ovotoxicity caused by 4-vinylcyclohexene diepoxide and 7, 12-dimethylbenz [a] anthracene in neonatal rat ovaries. Toxicol. Appl. Pharmacol. 241, 127-134.
31. Kim, J.H., Chu, S.C., Gramlich, J.L., Pride, Y.B., Babendreier, E., Chauhan, D., Salgia, R., Podar, K., Griffin, J.D., and Sattler, M. (2005). Activation of the PI3K/mTOR pathway by BCR-ABL contributes to increased production of reactive oxygen species. Blood 105, 1717-1723.
32. Klaunig, J.E., and Kamendulis, L.M. (2004). The role of oxidative stress in carcinogenesis. Annu. Rev. Pharmacol. Toxicol. 44, 239-267.
33. Matikainen, T., Perez, G.I., Zheng, T.S., Kluzak, T.R., Rueda, B.R., Flavell, R.A., and Tilly, J.L. (2001). Caspase-3 gene knockout defines cell lineage specificity for programmed cell death signaling in the ovary. Endocrinology 142, 2468-2480.
34. McGee, E.A., and Hsueh, A.J.W. (2000). Initial and cyclic recruitment of ovarian follicles. Endocr. Rev. 21, 200-214.
35. McLaughlin, E.A., and McIver, S.C. (2009). Awakening the oocyte: controlling primordial follicle development. Reproduction 137, 1-11.
36. Miller, K.P., Gupta, R.K., and Flaws, J.A. (2006). Methoxychlor metabolites may cause ovarian toxicity through estrogen-regulated pathways. Toxicol. Sci. 93, 180-188.
37. Morita, Y., Maravei, D.V., Bergeron, L., Wang, S., Perez, G.I., Tsutsumi, O., Taketani, Y., Asano, M., Horai, R., and Korsmeyer, S.J. (2001). Caspase-2 deficiency rescues female germ cells from death due to cytokine insufficiency but not meiotic defects caused by ataxia telangiectasia-mutated (Atm) gene inactivation. Cell Death Differ. 8, 614-620.
38. Muñiz, L. C., Yehia, G., Mémin, E., Ratnakar, P., and Molina, C.A. (2006). Transcriptional regulation of cyclin D2 by the PKA pathway and inducible cAMP early repressor in granulosa cells. Biol. Reprod. 75, 279-288.
39. Naughton, R., Quiney, C., Turner, S.D., and Cotter, T.G. (2009). Bcr-Abl-mediated redox regulation of the PI3K/AKT pathway. Leukemia 23, 1432-1440.
40. Neal, M.S., Zhu, J., Holloway, A.C., and Foster, W.G. (2007). Follicle growth is inhibited by benzo-[a]-pyrene, at concentrations representative of human exposure, in an isolated rat follicle culture assay. Hum. Reprod. 22, 961-967.
41. Paterson, M., Koothan, P.T., Morris, K.D., O'Byrne, K.T., Braude, P., Williams, A., and Aitken, R.J. (1992). Analysis of the contraceptive potential of antibodies against native and deglycosylated porcine ZP3 in vivo and in vitro. Biol. Reprod. 46, 523-534.
42. Perry, G., and Epel, D. (1985). Fertilization stimulates lipid peroxidation in the sea urchin egg* 1. Dev. Biol. 107, 58-65.
43. Powis, G., Svingen, B.A., and Appel, P. (1981). Quinone-stimulated superoxide formation by subcellular fractions, isolated hepatocytes, and other cells. Mol. Pharmacol. 20, 387-394.
44. Radjendirane, V., Joseph, P., Lee, Y.H., Kimura, S., Klein-Szanto, A.J.P., Gonzalez, F.J., and Jaiswal, A.K. (1998). Disruption of the DT diaphorase (NQO1) gene in mice leads to increased menadione toxicity. J. Biol. Chem. 273, 7382-7389.
45. Reddy, P., Adhikari, D., Zheng, W., Liang, S., Hamalainen, T., Tohonen, V., Ogawa, W., Noda, T., Volarevic, S., and Huhtaniemi, I. (2009). PDK1 signaling in oocytes controls reproductive aging and lifespan by manipulating the survival of primordial follicles. Hum. Mol. Genet. 18, 2813-2824.
46. Rucker, E.B., III., Dierisseau, P., Wagner, K.U., Garrett, L., Wynshaw-Boris, A., Flaws, J.A., and Hennighausen, L. (2000). Bcl-x and Bax regulate mouse primordial germ cell survival and apoptosis during embryogenesis. Mol. Endocrinol. 14, 1038-1052.
47. Scharer, C.D., McCabe, C.D., Ali-Seyed, M., Berger, M.F., Bulyk, M.L., and Moreno, C.S. (2009). Genome-wide promoter analysis of the SOX4 transcriptional network in prostate cancer cells. Cancer Res. 69, 709-717.
48. Sinner, D., Kordich, J.J., Spence, J.R., Opoka, R., Rankin, S., Lin, S.C.J., Jonatan, D., Zorn, A.M., and Wells, J.M. (2007). Sox17 and Sox4 differentially regulate {beta}-catenin/T-cell factor activity and proliferation of colon carcinoma cells. Mol. Cell. Biol. 27, 7802-7815.
49. Skinner, S.M., Mills, T., Kirchick, H.J., and Dunbar, B.S. (1984). Immunization with zona pellucida proteins results in abnormal ovarian follicular differentiation and inhibition of gonadotropin-induced steroid secretion. Endocrinology 115, 2418-2432.
50. Swain, J.E., and Smith, G.D. (2007). Reversible phosphorylation and regulation of mammalian oocyte meiotic chromatin remodeling and segregation. Soc. Reprod. Fertil. Suppl. 63, 343-358.
51. Tarin, J.J. (1996). Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Mol. Hum. Reprod. 2, 717-724.
52. Thompson, R.M., Gerber, N., Seibert, R.A., and Desiderio, D.M. (1972). Identification of 2-methyl-1, 4-naphthohydroguinone monoglucuronide as a metabolite of 2-methyl-1, 4-naphthoquinone (menadione) in rat bile. Res. Commun. Chem. Pathol. Pharmacol. 4, 543-552.
53. Wells, P.G., McCallum, G.P., Chen, C.S., Henderson, J.T., Lee, C.J.J., Perstin, J., Preston, T.J., Wiley, M.J., and Wong, A.W. (2009). Oxidative stress in developmental origins of disease: teratogenesis, neurodevelopmental deficits, and cancer. Toxicol. Sci. 108, 4-18.
54. Xing, W., and Sairam, M.R. (2002). Retinoic acid mediates transcriptional repression of ovine follicle-stimulating hormone receptor gene via a pleiotropic nuclear receptor response element. Biol. Reprod. 67, 204-211.