Siyami KARAHAN, Miyase ÇINAR, Aytül KÜRÜM, Hakan KOCAMIŞ, Emel ERGÜN

Determination of antioxidants in bovine oviduct epithelial cell culture isolated at different periods of the estrous cycle

Oxidative stress interferes with oviduct functions including oocyte maturation, capacitation, fertilization, and embryo andgamete transport. This study aimed to determine activity of the antioxidants glutathione peroxidase (GPX-I), superoxide dismutase(SOD), and catalase (CAT) in bovine oviduct epithelial cells (BOEC) isolated from the isthmus and ampulla of the oviduct at estral (n =7) and luteal phases (n = 7) of the estrous cycle. The antioxidant activity was measured at the primary, first, and second passages of thecell culture, and was characterized by cytokeratin expression. The GPX activity increased over the passages in samples of the ampullaand the isthmus of each sexual phase without statistical significance. The SOD activity remained steady through the cell passages inboth sexual phases. CAT activity at the primary culture was higher in the ampulla compared to the isthmus in both sexual phases witha significant difference for the estral phase (P < 0.05), and it decreased over the passages with no significant differences. In conclusion,the antioxidant enzyme activity profile of BOEC did not differ by region or sexual cycle except for that of CAT, which was higherin the ampulla. Further studies should focus on SOD, GPX, and CAT activity for the mechanism of BOEC adaptation to an in vitroenvironment.

PDF

___

1. Roy M, Gauvreau D, Bilodeau JF. Expression of superoxide dismutases in the bovine oviduct during the estrous cycle. Theriogenology 2008;70: 836-842.
2. Grippo AA, Way AL, Killian GJ. Effect of bovine ampullary and isthmic oviductal fluid on motility, acrosome reaction and fertility of bull spermatozoa. J Reprod Fertil 1995; 105: 57-64.
3. Abe H, Hoshi H. Bovine oviductal epithelial cells: Their cell culture and applications in studies for reproductive biology. Cytotechnology 1997; 23: 171-183.
4. Schoen J, Bondzio A, Topp K, Einspanier R. Establishment and characterization of an adherent pure epithelial cell line derived from the bovine oviduct. Theriogenology 2008; 69: 536-545.
5. Cerny KL, Garret E, Walton AJ, Anderson LH, Bridges PJ. A transcriptomal analysis of bovine oviductal epithelial cells collected during the follicular phase versus the luteal phase of the estrous cycle. Reprod Biol Endocrinol 2015; 13:84.
6. Mcnutt-Scott TL, Harris C. Modulation of intracellular glutathion and cysteine metabolism in bovine oviduct epithelial cells cultured in vitro. Biol Reprod 1998; 59: 314-320.
7. Agarwal A, Gupta S, Sharma RK. Role of oxidative stress in female reproduction. Reprod Biol Endocrinol 2005; 3: 28.
8. Agarwal A, Aponte-Mellado A, Premkumar BJ, Shaman A, Gupta S. The effects of oxidative stress on female reproduction: A review. Reprod Biol Endocrinol 2012; 10-49.
9. Ruder EH, Hartman TJ, Goldman MB. Impact of oxidative stress on female fertility. Curr Opin Obstet Gynecol. 2009; 21: 219-222.
10. Akkuş, İ. Serbest radikaller ve fizyopatolojik etkileri, Mimoza yayınları, (1995) Konya.
11. Davies KJA. Oxidative stress, antioxidant defenses, and damage removal, repair and replacement systems. IUBMB Life 2000; 50: 279-289.
12. Ho YS, Magnenat JL, Gargano M, Cao J. The nature of antioxidant defense mechanisms: a lesson from transgenic studies. Environ Health Perspect 1998; 5: 1219-1228.
13. Lapointe J, Bilodeau JF. Antioxidant defenses are modulated in the cow oviduct during the estrous cycle. Biol Reprod 2003; 68: 1157-1164.
14. Sanocka D, Kurpisz M. Reactive oxygen species and sperm cells. Reprod Biol Endocrinol 2004; 2-12.
15. Fujii J, Iuchi Y, Okada F. Fundamental roles of reactive oxygen species and protective mechanisms in the female reproductive system. Reprod Biol Endocrinol 2005; 3: 43.
16. Lapointe S, Sullivan R, Sirard MA. Binding of a bovine oviductal fluid catalase to mammalian spermatozoa. Biol Reprod 1998; 58: 747-753.
17. Lamirande E, Jiang H, Zini A, Kodama H, Gagnon C. Reactive oxygen species and sperm physiology. Rev Reprod 1997; 2: 48- 54.
18. Guthrie HD, Welch GR. Effect of reactive oxygen species on sperm function. Theriogenology 2012; 78: 1700-1708.
19. Henkel RR. Leukocytes and oxidative stress: dilemma for sperm function and male fertility. Asian J Androl 2011; 13: 43-52.
20. Agarwal A, Virk G, Ong C, Plesis SS. Effect of oxidative stress on male reproduction. World J Mens Health 2014; 32 (1): 1-17.
21. Wagner H, Cheng JW, Ko EY. Role of reactive oxygen species in male infertility: An update review of literature. Arab J Urol 2018; 16: 35-43.
22. O’Flaherty CM, Beorlegui NB, Beconi MT. Reactive oxygen species requirements for bovine sperm capacitation and acrosome reaction. Theriogenology 1999; 52: 289-301.
23. Ulbrich SE, Zitta K, Hiendleder S, Wolf E. In vitro systems for intercepting early embryo–maternal cross-talk in the bovine oviduct. Theriogenology 2010; 73: 802-816.
24. Monken de Assis P, Castro LS, Siqueira AFP, Delgado JC, Hamilton TRS, Goissis MD, Mendes CM, Nichi M, Visintin JA, Assumpção MEOA. System for evaluation of oxidative stress on in-vitro–produced bovine embryos. Reproductive Bio Medicine Online 2015; 31: 577-580.
25. Maillo V, Lopera-Vasquez R, Hamdi M, Gutierrez-Adan A, Lonergan P, Rizos D. Maternal–embryo interaction in the bovine oviduct: Evidence from in vivo and in vitro studies. Theriogenology 2016; 86: 443-450.
26. Jang HY, Ji SJ, Kim YH, Lee HY, Shin JS, Cheong HT, Kim JT, Park IC, Kong HS, Park CK et al. Antioxidative effects of astaxanthin against nitric oxide-induced oxidative stress on cell viability and gene expression in bovine oviduct epithelial cell and the developmental competence of bovine IVM/IVF embryos. Reprod Domest Anim 2010; 45: 967-974.
27. Jang HY, Jung YS, Cheong HT, Kim JT, Park CK, Kong HS, Lee HK, Yang BK. Effects of cell status of bovine oviduct epithelial cell (BOEC) on the development of bovine IVM/IVF embryos and gene expression in the BOEC used or not used for the embryo culture. Asian-Australas J Anim Sci 2008; 21 (7): 980- 987.
28. Cordova A, Perreau C, Uzbekova S, Ponsart C, Locatelli Y, Mermillod P. Development rate and gene expression of IVP bovine embryos cocultured with bovine oviduct epithelial cells at early or late stage of preimplantation development. Theriogenology 2014; 81 (9): 1163-1173.
29. Schmaltz-Panneaua B, Cordova A, Dhorne-Pollet S, Hennequet-Antier C, Uzbekovaa S, Martinot E, Doret S, Martin P, Mermillod P, Locatelli Y. Early bovine embryos regulate oviduct epithelial cell gene expression during in vitro co-culture. Anim Reprod Sci 2014; 149 (3-4): 103-116.
30. Lopera-Vásquez R, Hamdi M, Fernandez-Fuertes B, Maillo V, Beltrán-Breña P, Calle A, Redruello A, López-Martín S, Gutierrez-Adán A, Yañez-Mó M et al. Extracellular vesicles from BOEC in ın vitro embryo development and quality. PLos ONE 2016 11 (2): e0148083| DOI:10.1371/journal. pone.0148083.
31. Rąpała L, Starzyński RR, Trzeciak PZ, Dąbrowski S, Gajewska M, Jurka P, Smolarczyk R, Duszewska AM. Influence of elevated temperature on bovine oviduct epithelial cells (BOECs). PLos ONE 2018 15; 13 (6): e0198843. doi: 10.1371/ journal.pone.0198843.
32. Arosh JA, Parent J, Chapdelaine P, Sirois J, Fortier MA. Expression of cyclooxygenases 1 and 2 and prostaglandin E synthase in bovine endometrial tissue during the estrous cycle. Biol Reprod 2002; 67: 161-169.
33. Lee KF, Yeung WSB. Gamete/embryo-oviduct interactions: implications on in vitro culture. Hum Fertil 2006; 9: 137-143.
34. Walter, I. Culture of bovine oviduct epithelial cells (BOEC). Anat Rec 1995; 243: 347-356.
35. Rief S, Sinowatz F, Stojkovic M, Einspanier R, Wolf E, Prelle K. Effect of a novel co-culture system on development, metabolism and gene expression of bovine embryos produced in vitro. Reproduction 2002; 124: 543-556.
36. Harvey MB, Arcellana-Panlilio MY, Zhang X, Schultz GA, Watson AJ. Expression of genes encoding antioxidant enzymes in preimplantation mouse and cow embryos and primary bovine oviduct cultures employed for embryo coculture. Biol Reprod 1995 Sep; 53 (3): 532-540.
37. Mouatassim SE, Guerin P, Menezo Y. Mammalian oviduct and protection against free oxygen radicals: expression of genes encoding antioxidant enzymes in human and mouse. Eur J Obstet Gyn R B 2000; 89: 1-6.
38. Lapointe J, Kimmins S, Maclaren LA, Bilodeau JF. Estrogen selectively up-regulates the phospholipid hydroperoxide glutathione peroxidase in the oviducts. Endocrinology 2005 Jun; 146 (6): 2583-2592.
39. Georgiou AS, Sostaric E, Wong CH, Snijders APL, Wright PC, Moore HD, Fazeli A. Gametes alter the oviductal secretory proteome. Molecular & Cellular Protemics 2005; 4-11.
40. Pérez-Martínez C, García-Fernández RA, Escudero A, Ferreras MC, García-Iglesias MJ. Expression of cytokeratins and vimentin in normal and neoplastic tissue from the bovine female reproductive tract. J Comp Pathol. 2001; 124 (1): 70-78.
41. Halliwell B. Cell culture, oxidative stress, and antioxidants: Avoiding pitfalls. Biomed J 2014; 37: 99-105.
42. Reis AN, Silva, LKX, Silva AOA, Sousa JS, Vale WG. Effect of estradiol and progesterone on development and quality of bovine embryos produced in vitro. Arq Bras Med Vet Zootec 2010; 62: 1375-1380.