Journal of Animal Reproduction and Biotechnology (한국동물생명공학회지)

The Korean Society of Animal Reproduction and Biotechnology (한국동물생명공학회)
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Immunohistological expression of cytochrome P450 1A2 (CYP1A2) in the ovarian follicles of prepubertal and pubertal rat

  • Hwang, Jong-Chan (College of Veterinary Medicine, Kyungpook National University) ;
  • Park, Byung-Joon (College of Veterinary Medicine, Kyungpook National University) ;
  • Kim, Hwan-Deuk (College of Veterinary Medicine, Kyungpook National University) ;
  • Baek, Su-Min (College of Veterinary Medicine, Kyungpook National University) ;
  • Lee, Seoung-Woo (College of Veterinary Medicine, Kyungpook National University) ;
  • Jeon, Ryoung-Hoon (College of Veterinary Medicine, Gyeongsang National University) ;
  • Jang, Min (College of Veterinary Medicine, Kyungpook National University) ;
  • Bae, Seul-Gi (College of Veterinary Medicine, Kyungpook National University) ;
  • Yun, Sung-Ho (College of Veterinary Medicine, Kyungpook National University) ;
  • Park, Jin-Kyu (College of Veterinary Medicine, Kyungpook National University) ;
  • Kwon, Young-Sam (College of Veterinary Medicine, Kyungpook National University) ;
  • Kim, Seung-Joon (College of Veterinary Medicine, Kyungpook National University) ;
  • Lee, Won-Jae (College of Veterinary Medicine, Kyungpook National University)
  • Received : 2020.12.03
  • Accepted : 2020.12.14
  • Published : 2020.12.31
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Abstract

Cytochrome P450 1A2 (CYP1A2) is a member of the cytochrome P450 superfamily enzymes in mammals and plays a major role in metabolizing endogenous hormones in the liver. In recent days, CYP1A2 expression has been found in not only the liver but also other tissues including the pancreas and lung. However, little information is available regarding the expression of CYP1A2 in the ovary, in spite of the facts that the ovarian follicle growth and atresia are tightly associated with controls of endocrine hormonal networks. Therefore, the expression of CYP1A2 in the ovaries of prepubertal and pubertal rats was investigated to assess its expression pattern and puberty-related alteration. It was demonstrated that the expression level of CYP1A2 was significantly (p < 0.01) higher in the pubertal ovaries than prepubertal counterparts. At the ovarian follicle level in both groups, whereas CYP1A2 expression was less detectable in the primordial, primary and secondary follicles, the strongly positive expression of CYP1A2 was localized in the granulosa cell layers in the antral and pre-ovulatory follicles. However, the ratio of CYP1A2-positive ovarian follicle was significantly (p < 0.01) higher in the ovary of pubertal group (73.1 ± 3.1%) than prepubertal one (41.0 ± 10.5%). During the Immunofluorescence, expression of CYP1A2 was mainly localized in Fas-positive follicles, indicating the atretic follicles. In conclusion, these results suggested that CYP1A2 expression was mainly localized at the atretic follicular cells and affected by the onset of puberty. Further study is still necessary but we hypothesize that CYP1A2 expresses in the atretic follicles to metabolize residue of the reproductive hormones. These findings may have important implications for the fields of reproductive biology of animals.

Keywords

References

  1. Cannady EA, Dyer CA, Christian PJ, Sipes IG, Hoyer PB. 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. https://doi.org/10.1093/toxsci/kfg077
  2. Dasmahapatra AK, Trewin AL, Hutz RJ. 2002. Estrous cycle-regulated expression of CYP1B1 mRNA in the rat ovary. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 133:127-134. https://doi.org/10.1016/S1096-4959(02)00119-7
  3. Dey A, Jones JE, Nebert DW. 1999. Tissue- and cell type-specific expression of cytochrome P450 1A1 and cytochrome P450 1A2 mRNA in the mouse localized in situ hybridization. Biochem. Pharmacol. 58:525-537. https://doi.org/10.1016/S0006-2952(99)00110-0
  4. Downie D, McFadyen MC, Rooney PH, Cruickshank ME, Parkin DE, Miller ID, Telfer C, Melvin WT, Murray GI. 2005. Profiling cytochrome P450 expression in ovarian cancer: identification of prognostic markers. Clin. Cancer Res. 11:7369-7375. https://doi.org/10.1158/1078-0432.CCR-05-0466
  5. Gaytan F, Morales C, Leon S, Heras V, Barroso A, Avendano MS, Vazquez MJ, Castellano JM, Roa J, Tena-Sempere M. 2017. Development and validation of a method for precise dating of female puberty in laboratory rodents: the puberty ovarian maturation score (Pub-Score). Sci. Rep. 7:46381. https://doi.org/10.1038/srep46381
  6. Gershon E and Dekel N. 2020. Newly identified regulators of ovarian folliculogenesis and ovulation. Int. J. Mol. Sci. 21:4565. https://doi.org/10.3390/ijms21124565
  7. Guengerich FP. 2013. New trends in cytochrome p450 research at the half-century mark. J. Biol. Chem. 288:17063-17064. https://doi.org/10.1074/jbc.R113.466821
  8. Kim SJ. 2019. The chronic and unpredictable stress suppressed kisspeptin expression during ovarian cycle in mice. J. Anim. Reprod. Biotechnol. 34:40-49. https://doi.org/10.12750/jarb.34.1.40
  9. Lee HJ, Jeon RH, Park BJ, Jang SJ, Lee SL, Rho GJ, Kim SJ, Lee WJ. 2019. Differentiation inductions altered telomere length and telomerase activity in human dental pulp-derived mesenchymal stem cell. J. Anim. Reprod. Biotechnol. 34:93-99. https://doi.org/10.12750/JARB.34.2.93
  10. Lee SY, Oh SJ, Yun KU, Kim HM, Kim BH, Lee K, Kim SK. 2012. Expression of hepatic and ovarian cytochrome P450 during estrous cycle in rats. Arch. Toxicol. 86:75-85. https://doi.org/10.1007/s00204-011-0730-1
  11. Leighton JK, Canning S, Guthrie HD, Hammond JM. 1995. Expression of cytochrome P450 1A1, an estrogen hydroxylase, in ovarian granulosa cells is developmentally regulated. J. Steroid Biochem. Mol. Biol. 52:351-356. https://doi.org/10.1016/0960-0760(94)00185-O
  12. Li J, Gao H, Tian Z, Wu Y, Wang Y, Fang Y, Lin L, Han Y, Wu S, Haq I, Zeng S. 2016. Effects of chronic heat stress on granulosa cell apoptosis and follicular atresia in mouse ovary. J. Anim. Sci. Biotechnol. 7:57. https://doi.org/10.1186/s40104-016-0116-6
  13. Lin J, Zheng J, Zhang H, Chen J, Yu Z, Chen C, Xiong Y, Liu T. 2018. Cytochrome P450 family proteins as potential biomarkers for ovarian granulosa cell damage in mice with premature ovarian failure. Int. J. Clin. Exp. Pathol. 11:4236-4246.
  14. Lu J, Shang X, Zhong W, Xu Y, Shi R, Wang X. 2020. New insights of CYP1A in endogenous metabolism: a focus on single nucleotide polymorphisms and diseases. Acta Pharm. Sin. B 10:91-104. https://doi.org/10.1016/j.apsb.2019.11.016
  15. Matsuda F, Inoue N, Manabe N, Ohkura S. 2012. Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells. J. Reprod. Dev. 58:44-50. https://doi.org/10.1262/jrd.2011-012
  16. Mayer C, Acosta-Martinez M, Dubois SL, Wolfe A, Radovick S, Boehm U, Levine JE. 2010. Timing and completion of puberty in female mice depend on estrogen receptor alpha-signaling in kisspeptin neurons. Proc. Natl. Acad. Sci. U. S. A. 107:22693-22698. https://doi.org/10.1073/pnas.1012406108
  17. McDonnell AM and Dang CH. 2013. Basic review of the cytochrome p450 system. J. Adv. Pract. Oncol. 4:263-268.
  18. Mercurio MG, Shiff SJ, Galbraith RA, Sassa S. 1995. Expression of cytochrome P450 mRNAs in the colon and the rectum in normal human subjects. Biochem. Biophys. Res. Commun. 210:350-355. https://doi.org/10.1006/bbrc.1995.1668
  19. Mikhailova ON, Gulyaeva LF, Prudnikov AV, Gerasimov AV, Krasilnikov SE. 2006. Estrogen-metabolizing gene polymorphisms in the assessment of female hormone-dependent cancer risk. Pharmacogenomics J. 6:189-193. https://doi.org/10.1038/sj.tpj.6500365
  20. Nishimura M, Yaguti H, Yoshitsugu H, Naito S, Satoh T. 2003. Tissue distribution of mRNA expression of human cytochrome P450 isoforms assessed by high-sensitivity real-time reverse transcription PCR. Yakugaku Zasshi 123:369-375. https://doi.org/10.1248/yakushi.123.369
  21. Omiecinski CJ, Redlich CA, Costa P. 1990. Induction and developmental expression of cytochrome P450IA1 messenger RNA in rat and human tissues: detection by the polymerase chain reaction. Cancer Res. 50:4315-4321.
  22. Rivest RW. 1991. Sexual maturation in female rats: hereditary, developmental and environmental aspects. Experientia 47:1027-1038. https://doi.org/10.1007/BF01923338
  23. Shan X, Yu T, Yan X, Wu J, Fan Y, Guan X, Fang F, Lin Y, Zhang Y, Li Y, Liu Y. 2020. Proteomic analysis of healthy and atretic porcine follicular granulosa cells. J. Proteomics 31:104027.
  24. Sugiyama S, Uno Y, Amano T, Kitazawa T, Teraoka H. 2019. Genetic diversity of cytochrome P450 1A2 with different metabolic activities in domestic cats. J. Vet. Med. Sci. 81:980-982. https://doi.org/10.1292/jvms.19-0106
  25. Symonds DA, Miller KP, Tomic D, Flaws JA. 2006. Effect of methoxychlor and estradiol on cytochrome p450 enzymes in the mouse ovarian surface epithelium. Toxicol. Sci. 89:510-514. https://doi.org/10.1093/toxsci/kfj044
  26. Takagi K, Yamada T, Miki Y, Umegaki T, Nishimura M, Sasaki J. 2007. Histological observation of the development of follicles and follicular atresia in immature rat ovaries. Acta Med. Okayama 61:283-298.
  27. Uenoyama Y, Inoue N, Maeda KI, Tsukamura H. 2018. The roles of kisspeptin in the mechanism underlying reproductive functions in mammals. J. Reprod. Dev. 64:469-476. https://doi.org/10.1262/jrd.2018-110
  28. Vukovic V, Ianuale C, Leoncini E, Pastorino R, Gualano MR, Amore R, Boccia S. 2016. Lack of association between polymorphisms in the CYP1A2 gene and risk of cancer: evidence from meta-analyses. BMC Cancer 16:83. https://doi.org/10.1186/s12885-016-2096-5
  29. Wijnen PA, Op den Buijsch RA, Drent M, Kuijpers PM, Neef C, Bast A, Bekers O, Koek GH. 2007. Review article: the prevalence and clinical relevance of cytochrome P450 polymorphisms. Aliment. Pharmacol. Ther. 26 Suppl 2:211-219. https://doi.org/10.1111/j.1365-2036.2007.03490.x
  30. Yu YS, Sui HS, Han ZB, Li W, Luo MJ, Tan JH. 2004. Apoptosis in granulosa cells during follicular atresia: relationship with steroids and insulin-like growth factors. Cell Res. 14:341-346. https://doi.org/10.1038/sj.cr.7290234
  31. Zhang J, Liu Y, Yao W, Li Q, Liu H, Pan Z. 2018. Initiation of follicular atresia: gene networks during early atresia in pig ovaries. Reproduction 156:23-33. https://doi.org/10.1530/REP-18-0058
  32. Zhou J, Peng X, Mei S. 2019. Autophagy in ovarian follicular development and atresia. Int. J. Biol. Sci. 15:726-737. https://doi.org/10.7150/ijbs.30369