Understanding the villain: DMBA-induced preantral ovotoxicity involves selective follicular destruction and primordial follicle activation through PI3K/Akt and mTOR signaling

Toxicological Sciences

Volumn 123, Issue 2, 2011, Pages 563-575

  Sobinoff, Alexander P ^a   Mahony, Michelle ^a   Nixon, Brett ^a,b   Roman, Shaun D ^a,b   Mclaughlin, Eileen A ^a,b  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

DMBA; Fertility; Ovary; PI3K Akt mTOR signaling; Primordial follicle

Indexed keywords

DIMETHYLBENZ[A]ANTHRACENE; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL ACTIVATION; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; MOLECULAR MECHANICS; NEWBORN; NONHUMAN; OOCYTE; OVARY DISEASE; OVARY FOLLICLE; OVARY FOLLICLE ATRESIA; OVOTOXICITY; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; TOXICITY; UPREGULATION;

9,10-DIMETHYL-1,2-BENZANTHRACENE; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; CARCINOGENS; CELLS, CULTURED; FEMALE; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ONCOGENE PROTEIN V-AKT; OVARIAN FOLLICLE; PHOSPHATIDYLINOSITOL 3-KINASES; RNA, MESSENGER; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; UP-REGULATION;

RATTUS;

EID: 80053457043     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr195     Document Type: Article

References (51)

1. Adhikari, D., Zheng, W., Shen, Y., Gorre, N., Hamalainen, T., Cooney, A. J., Huhtaniemi, I., Lan, Z. J., and Liu, K. (2010). Tsc/mTORC 1 signaling in oocytes governs the quiescence and activation of primordial follicles. Hum. Mol. Genet. 19, 397-410.
2. Agashe, V. R., and Hartl, F. U. (2000). Roles of molecular chaperones in cytoplasmic protein folding. Semin. Cell Dev. Biol. 11, 15-25.
3. Arnaud, E., Touriol, C., Boutonnet, C., Gensac, M. C., Vagner, S., Prats, H., and Prats, A. C. (1999). A new 34-kilodalton isoform of human fibroblast growth factor 2 is cap dependently synthesized by using a non-AUG start codon and behaves as a survival factor. Mol. Cell. Biol. 19, 505-514.
4. Baker, D. J., Dawlaty, M. M., Galardy, P., and Van Deursen, J. M. (2007). Mitotic regulation of the anaphase-promoting complex. Cell. Mol. Life Sci. 64, 589-600.
5. Baksh, S., Widlund, H. R., Frazer-Abel, A. A., Du, J., Fosmire, S., Fisher, D. E., DeCaprio, J. A., Modiano, J. F., and Burakoff, S. J. (2002). NFATc2-mediated repression of cyclin-dependent kinase 4 expression. Mol. Cell 10, 1071-1081.
6. Barua, A., and Yoshimura, Y. (1999). Immunolocalization of MHC-II{thorn} cells in the ovary of immature, young laying and old laying hens Gallus domesticus. J. Reprod. Fertil. 116, 385-389.
7. Blachère, N. E., Darnell, R. B., and Albert, M. L. (2005). Apoptotic cells deliver processed antigen to dendritic cells for cross-presentation. PLoS Biol. 3, 1070.
8. 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.
9. Cheng, S. W. Y., Fryer, L. G. D., Carling, D., and Shepherd, P. R. (2004). Thr2446 is a novel mammalian target of rapamycin (mTOR) phosphorylation site regulated by nutrient status. J. Biol. Chem. 279, 15719-15722.
10. Chomczynski, P., and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
11. Coulam, C. B., Adamson, S. C., and Annegers, J. F. (1986). Incidence of premature ovarian failure. Obstet. Gynecol. 67, 604-606.
12. Crist, K. A., Zhang, Z., You, M., Gunning, W. T., Conran, P. B., Steele, V. E., and Lubet, R. A. (2005). Characterization of rat ovarian adenocarcinomas developed in response to direct instillation of 7, 12-dimethylbenz[a]-anthracene (DMBA) coated suture. Carcinogenesis 26, 951-957.
13. Dai, Y. S., Xu, J., and Molkentin, J. D. (2005). The DnaJ-related factor Mrj interacts with nuclear factor of activated T cells c3 and mediates transcriptional repression through class II histone deacetylase recruitment. Mol. Cell. Biol. 25, 9936-9948.
14. Diamond, R. H., Du, K., Lee, V. M., Mohn, K. L., Haber, B. A., Tewari, D. S., and Taub, R. (1993). Novel delayed-early and highly insulin-induced growth response genes. Identification of HRS, a potential regulator of alternative pre-mRNA splicing. J. Biol. Chem. 268, 15185-15192.
15. Diehl, J. A., Yang, W., Rimerman, R. A., Xiao, H., and Emili, A. (2003). Hsc70 regulates accumulation of cyclin D1 and cyclin D1-dependent protein kinase. Mol. Cell. Biol. 23, 1764-1774.
16. Du, X. L., Yang, H., Liu, S. G., Luo, M. L., Hao, J. J., Zhang, Y., Lin, D. C., Xu, X., Cai, Y., and Zhan, Q. M. (2009). Calreticulin promotes cell motility and enhances resistance to anoikis through STAT3-CTTN-Akt pathway in esophageal squamous cell carcinoma. Oncogene 28, 3714-3722.
17. Fuller-Pace, F. V., and Moore, H. C. (2011). RNA helicases p68 and p72: multifunctional proteins with important implications for cancer development. Future Oncol. 7, 239-251.
18. Gelboin, H. V. (1980). Benzo [alpha] pyrene metabolism, activation and carcinogenesis: role and regulation of mixed-function oxidases and related enzymes. Physiol. Rev. 60, 1107-1166.
19. Hashimoto, T., Yanaihara, N., Okamoto, A., Nikaido, T., Saito, M., Takakura, S., Yasuda, M., Sasaki, H., Ochiai, K., and Tanaka, T. (2011). Cyclin D1 predicts the prognosis of advanced serous ovarian cancer. Exp. Ther. Med. 2, 213-219.
20. Hirshfield, A. N. (1991). Development of follicles in the mammalian ovary. Int. Rev. Cytol. 124, 43-101.
21. Hoyer, P. B., Davis, J. R., Bedrnicek, J. B., Marion, S. L., Christian, P. J., Barton, J. K., and Brewer, M. A. (2009). Ovarian neoplasm development by 7, 12-dimethylbenz [a] anthracene (DMBA) in a chemically-induced rat model of ovarian failure. Gynecol. Oncol. 112, 610-615.
22. Hoyer, P. B., and Sipes, I. G. (1996). Assessment of follicle destruction in chemical-induced ovarian toxicity. Annu. Rev. Pharmacol. Toxicol. 36, 307-331.
23. Huang, C. S., Shen, C. Y., Wang, H. W., Wu, P. E., and Cheng, C. W. (2007). Increased expression of SRp40 affecting CD44 splicing is associated with the clinical outcome of lymph node metastasis in human breast cancer. Clin. Chim. Acta 384, 69-74.
24. Huez, I., Créancier, L., Audigier, S., Gensac, M. C., Prats, A. C., and Prats, H. (1998). Two independent internal ribosome entry sites are involved in translation initiation of vascular endothelial growth factor mRNA. Mol. Cell. Biol. 18, 6178-6190.
25. Igawa, Y., Keating, A. F., Rajapaksa, K. S., Sipes, I. G., and Hoyer, P. B. (2009). Evaluation of ovotoxicity induced by 7, 12-dimethylbenz [a] anthracene and its 3, 4-diol metabolite utilizing a rat in vitro ovarian culture system. Toxicol. Appl. Pharmacol. 234, 361-369.
26. Keating, A. F., Fernandez, S. M., Mark-Kappeler, C. J., Sen, N., Sipes, I. G., and Hoyer, P. B. (2010). Inhibition of PIK3 signaling pathway members by the ovotoxicant 4-vinylcyclohexene diepoxide in rats. Biol. Reprod. 84, 743-751.
27. Kim, K. K., Shim, J. C., and Kim, J. R. (2003). Overexpression of p21, cyclin E and decreased expression of p27 in DMBA (7, 12 dimethylbenzanthracene) induced rat ovarian carcinogenesis. Pathol. Int. 53, 291-296.
28. Koloteva-Levine, N., Pinchasi, D., Pereman, I., Zur, A., Brandeis, M., and Elroy-Stein, O. (2004). The Apc5 subunit of the anaphase-promoting complex/cyclosome interacts with poly (A) binding protein and represses internal ribosome entry site-mediated translation. Mol. Cell. Biol. 24, 3577-3587.
29. Martherus, R. S. R. M., and Sluiter, W. (2010). Functional annotation of heart enriched mitochondrial genes GBAS and CHCHD10 through guilt by association. Biochem. Biophys. Res. Commun. 402(2), 203-208.
30. Martineau, Y., Le Bec, C., Monbrun, L., Allo, V., Chiu, I. M., Danos, O., Moine, H., Prats, H., and Prats, A. C. (2004). Internal ribosome entry site structural motifs conserved among mammalian fibroblast growth factor 1 alternatively spliced mRNAs. Mol. Cell. Biol. 24, 7622-7635.
31. Mattison, D. R., and Schulman, J. D. (1980). How xenobiotic chemicals can destroy oocytes. Contemp. Obstet. Gynecol. 15, 157-169.
32. McGee, E. A., and Hsueh, A. J. W. (2000). Initial and cyclic recruitment of ovarian follicles. Endocr. Rev. 21, 200-214.
33. McLaughlin, E. A., and McIver, S. C. (2009). Awakening the oocyte: controlling primordial follicle development. Reproduction 137, 1-11.
34. Moskovitz, J., Berlett, B. S., Poston, J. M., and Stadtman, E. R. (1997). The yeast peptide-methionine sulfoxide reductase functions as an antioxidant in vivo. Proc. Natl. Acad. Sci. U.S.A. 94, 9585-9589.
35. Muñiz, L. C., Yehia, G., Mémin, E., Ratnakar, P. V. A. L., 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.
36. Nauta, A. J., Daha, M. R., Kooten, C., and Roos, A. (2003). Recognition and clearance of apoptotic cells: a role for complement and pentraxins. Trends Immunol. 24, 148-154.
37. Nicol, S. M., and Fuller-Pace, F. V. (2010). Analysis of the RNA helicase p68 (Ddx5) as a transcriptional regulator. Methods Mol. Biol. 587, 265-279.
38. Pati, D., Keller, C., Groudine, M., and Plon, S. E. (1997). Reconstitution of a MEC1-independent checkpoint in yeast by expression of a novel human fork head cDNA. Mol. Cell. Biol. 17, 3037-3046.
39. Polak, P., and Hall, M. N. (2006). mTORC2 caught in a SINful Akt. Dev. Cell 11, 433-434.
40. 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.
41. Reddy, P., Zheng, W., and Liu, K. (2010). Mechanisms maintaining the dormancy and survival of mammalian primordial follicles. Trends Endocrinol. Metab. 21, 96-103.
42. Robker, R. L., and Richards, J. A. S. (1998). Hormone-induced proliferation and differentiation of granulosa cells: a coordinated balance of the cell cycle regulators cyclin D2 and p27Kip1. Mol. Endocrinol. 12, 924-940.
43. Scott, K. L., and Plon, S. E. (2005). CHES1/FOXN3 interacts with Skiinteracting protein and acts as a transcriptional repressor. Gene 359, 119-126.
44. Sobinoff, A. P., Pye, V., Nixon, B., Roman, S. D., and McLaughlin, E. A. (2010). Adding insult to injury: effects of xenobiotic induced preantral ovotoxicity on ovarian development and oocyte fusibility. Toxicol. Sci 118(2), 653-666.
45. Tsai-Turton, M., Nakamura, B. N., and Luderer, U. (2007). Induction of apoptosis by 9, 10-dimethyl-1, 2-benzanthracene in cultured preovulatory rat follicles is preceded by a rise in reactive oxygen species and is prevented by glutathione. Biol. Reprod. 77, 442-451.
46. Vanoverberghe, K., Abeele, F. V., Mariot, P., Lepage, G., Roudbaraki, M., Bonnal, J. L., Mauroy, B., Shuba, Y., Skryma, R., and Prevarskaya, N. (2003). Ca2+ homeostasis and apoptotic resistance of neuroendocrinedifferentiated prostate cancer cells. Cell Death Differ. 11, 321-330.
47. Vericat, J. A., Cheng, S. C., and Dipple, A. (1989). Absolute stereochemistry of the major 7, 12-dimethylbenz (a) anthracene-DNA adducts formed in mouse cells. Carcinogenesis 10, 567-570.
48. Vougas, K., Gaitanarou, E., Marinos, E., Kittas, C., and Voloudakis-Baltatzis, I. E. (2008). Two-dimensional electrophoresis and immunohistochemical study of calreticulin in colorectal adenocarcinoma and mirror biopsies. J. BUON 13, 101-107.
49. Wang,Q., Zhou,Y., Jackson, L. N., Johnson, S.M., Chow,C.W., and Evers,B.M. (2011). Nuclear factor of activated T cells (NFAT) signaling regulates PTEN expression and intestinal cell differentiation. Mol. Biol. Cell 22, 412-420.
50. Wang, X. Y., Smith, D. I., Liu, W., and James, C. D. (1998). GBAS, a novel gene encoding a protein with tyrosine phosphorylation sites and a transmembrane domain, is co-amplified with EGFR. Genomics 49, 448-451.
51. Zhang, D. X., Li, X. P., Sun, S. C., Shen, X. H., Cui, X. S., and Kim, N. H. (2010). Involvement of ER-calreticulin-Ca2+ signaling in the regulation of porcine oocyte meiotic maturation and maternal gene expression. Mol. Reprod. Dev. 77, 462-471.