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http://dx.doi.org/10.12750/JARB.34.3.222

Effects of Eicosapentaenoic Acid during In Vitro Maturation of Porcine Oocytes: Hormone Synthesis and Embryonic Developmental Potential  

Kim, Kang-Sig (Ellemedi Obstetrics and Gynecology)
Park, Hum-Dai (Department of Biotechnology, Daegu University)
Publication Information
Journal of Animal Reproduction and Biotechnology / v.34, no.3, 2019 , pp. 222-231 More about this Journal
Abstract
Among fatty acid families, the polyunsaturated fatty acids were demonstrated to be mediators in various reproductive processes as precursor of steroid hormone (via cholesterol) and prostaglandins (via arachidonic acid), and in the last decade, major research was focused on the effects of omega-6 and especially omega-3 fatty acid. Eicosapentaenoic acid, the longest members of omega-3 fatty acid family, can be produced by a series of desaturation and elongation reactions from shorter member such as α-Linolenic acid. However, very few studies have provided detailed descriptions of Eicosapentaenoic acid effects and mechanisms of action in mammalian oocytes. The purpose of this study was to evaluate the effect of Eicosapentaenoic acid supplementation on in vitro maturation and developmental potential of porcine oocytes. Various concentrations of Eicosapentaenoic acid was added into in vitro maturation medium, and we evaluated the degree of cumulus expansion, nuclear maturation rate, blastocysts quality, and levels of prostaglandin E2, 17β-estradiol, progesterone in the spent medium. High doses (100 μM) of Eicosapentaenoic acid supplementation significantly inhibited cumulus expansion and oocyte nuclear maturation, and prostaglandin E2 synthesis also significantly decreased compared with other groups (p < 0.05). Supplementation of 50 μM Eicosapentaenoic acid showed higher quality blastocysts in terms of high cell numbers and low apoptosis when compared with other groups (p < 0.05), and synthesis ratio of E2/P4 also significantly increased compared with control group (p < 0.05). However, Supplementation of 100 μM Eicosapentaenoic acid showed high apoptosis when compared with other groups (p < 0.05), and synthesis ratio of 17β-estradiol/progesterone also significantly decreased compared with control group (p < 0.05). Our results indicated that supplementation with appropriate levels of Eicosapentaenoic acid beneficially affects the change of hormone synthesis for controlling oocyte maturation, leading to improved embryo quality. However, high doses of Eicosapentaenoic acid treatment results in detrimental effects.
Keywords
Eicosapentaenoic acid; porcine oocytes; prostaglandin; $17{\beta}$-estradiol/progesterone;
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1 Aardema H, Roelen BA, van Tol HT, Oei CH, Gadella BM, Vos PL. 2013. Follicular $17{\beta}$-estradiol and progesterone concentrations and degree of cumulus cell expansion as predictors of in vivo-matured oocyte developmental competence in superstimulated heifers. Theriogenology. 80:576-583.   DOI
2 Abayasekara DR, Wathes DC. 1999. Effects of altering dietary fatty acid composition on PG synthesis and fertility. PGs Leukot Essent Fatty Acids. 61:275-287.   DOI
3 Abeydeera LR, Day BN. 1997. In vitro penetration of pig oocytes in a modifidied tris-buffered medium: effect of BSA, caffeine and calcium. Theriogenology. 48:537-544.   DOI
4 Andrade LN, de Lima TM, Curi R, Castrucci AM. 2005. Toxicity of fatty acids on murine and human melanoma cell lines. Toxicol. In Vitro. 19:553-560.   DOI
5 Beker-van Woudenberg AR, van Tol HT, Roelen BA, Colenbrander B, Bevers MM. 2004. Estradiol and its membraneimpermeable conjugate (estradiol-bovine serum albumin) during in vitro maturation of bovine oocytes: effects on nuclear and cytoplasmic maturation, cytoskeleton, and embryo quality. Biol Reprod. 70:1465-1474.   DOI
6 Bilby TR, Jenkins T, Staples CR, Thatcher WW. 2006. Pregnancy, bovine somatotropin, and dietary n-3 fatty acids in lactating dairy cows: III. Fatty acid distribution. J. Dairy Sci. 89:3386-3399.   DOI
7 Childs S, Hennessy AA, Sreenan JM, Wathes DC, Cheng Z, Stanton C, Diskin MG, Kenny DA. 2008. Effect of level of dietary n-3 polyunsaturated fatty acid supplementation on systemic and tissue fatty acid concentrations and on selected reproductive variables in cattle. Theriogenology. 70:595-611.   DOI
8 Eppig JJ. 1981. PG E2 stimulates cumulus expansion and hyaluronic acid synthesis by cumuli oophori isolated from mice. Biol. Reprod. 25:191-195.   DOI
9 Ghaffarilaleh V, Fouladi-Nashta A, Paramio MT. 2014. Effect of $\alpha$-linolenic acid on oocyte maturation and embryo development of prepubertal sheep oocytes. Theriogenology 82:686-696.   DOI
10 Gulliver CE, Friend MA, King BJ, Clayton EH. 2012. The role of omega-3 polyunsaturated fatty acids in reproduction of sheep and cattle. Anim. Reprod. Sci. 131:9-22.   DOI
11 Hizaki H, Segi E, Sugimoto Y, Hirose M, Saji T, Ushikubi F, Matsuoka T, Noda Y, Tanaka T, Yoshida N, Narumiya S, Ichikawa A. 1999. Abortive expansion of the cumulus and impaired fertility in mice lacking the PG E receptor subtype EP(2). Proc. Natl. Acad. Sci. 96:10501-10506.   DOI
12 Hyttel P, Callesen H, Greve T. 1986. Ultrastructural features of preovulatory oocyte maturation in superovulated cattle. J. Reprod. Fertil. 76:645-656.   DOI
13 Ireland JJ, Roche JF. 1983. Growth and differentiation of large antral follicles after spontaneous luteolysis in heifers: changes in concentration of hormones in follicular fluid and specific binding of gonadotropins to follicles. J. Anim. Sci. 57:157-167.   DOI
14 Lands WE. 1992. Biochemistry and physiology of n-3 fatty acids. FASEB J. 6:2530-2536.   DOI
15 Maya-Soriano MJ, Lopez-Gatius F, Andreu-Vazquez C, Lopez-Bejar M. 2013. Bovine oocytes show a higher tolerance to heat shock in the warm compared with the cold season of the year. Theriogenology. 79:299-305.   DOI
16 Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O. 1993. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc. Natl. Acad. Sci. 90:11162-11166.   DOI
17 Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, Montgomery Jr CA, et al. 1995. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev. 9:2266-2278.   DOI
18 Marei WF, Wathes DC, Fouladi-Nashta AA. 2009. The effect of linolenic Acid on bovine oocyte maturation and development. Biol. Reprod. 81:1064-1072.   DOI
19 Moallem U, Shafran A, Zachut M, Dekel I, Portnick Y, Arieli A. 2013. Dietary $\alpha$-linolenic acid from flaxseed oil improved folliculogenesis and IVF performance in dairy cows, similar to eicosapentaenoic and docosahexaenoic acids from fish oil. Reproduction. 146:603-614.   DOI
20 Modina SC, Tessaro I, Lodde V, Franciosi F, Corbani D, Luciano AM. 2014. Reductions in the number of mid-sized antral follicles are associated with markers of premature ovarian senescence in dairy cows. Reprod. Fertil. Dev. 26:235-244.   DOI
21 Neal P, Baker TG, McNatty KP, Scaramuzzi RJ. 1975. Influence of PGs and human chorionic gonadotrophin on progesterone concentration and oocyte maturation in mouse ovarian follicles maintained in organ culture. J. Endocrinol. 65:19-25.   DOI
22 Petters RM, Wells KD. 1993. Culture of pig embryos. [Review]. J. Reprod. Fertil. Suppl. 48:61-73.
23 Nuttinck F, Gall L, Ruffini S, Laffont L, Clement L, Reinaud P. 2011. PTGS2-related $PGE_2$ affects oocyte MAPK phosphorylation and meiosis progression in cattle: late effects on early embryonic development. Biol. Reprod. 84:1248-1257.   DOI
24 Oseikria M, Elis S, Maillard V, Corbin E, Uzbekova S. 2016. N-3 polyunsaturated fatty acid DHA during IVM affected oocyte developmental competence in cattle. Theriogenology 85:1625-1634.   DOI
25 Petit HV, Germiquet C, Lebel D. 2004. Effect of feeding whole, unprocessed sunflower seeds and flaxseed on milk production, milk composition, and PG secretion in dairy cows. J. Dairy Sci. 87:3889-3898.   DOI
26 Roberts AJ, Skinner MK. 1990. Estrogen regulation of thecal cell steroidogenesis and differentiation: thecal cell-granulosa cell interactions. Endocrinology. 127:2918-2929.   DOI
27 Robinson R, Pushpakumara P, Cheng Z, Peters A, Abayasekara D, Wathes D. 2002. Effects of dietary polyunsaturated fatty acids on ovarian and uterine function in lactating dairy cows. Reproduction. 124:119-131.   DOI
28 Sargent JR. 1997. Fish oils and human diet. Br. J. Nutr. 78:5-13.   DOI
29 Scorletti E, Byrne CD. 2013. "Omega-3 fatty acids, hepatic lipid metabolism, and nonalcoholic fatty liver disease". Annual Review of Nutrition. 33:231-248.   DOI
30 Siqueira LC, Barreta MH, Gasperin B, Bohrer R, Santos JT, Buratini Jr J, et al. 2012. Angiotensin II, progesterone, and prostaglandins are sequential steps in the pathway to bovine oocyte nuclear maturation. Theriogenology 77:1779-1187.   DOI
31 Walsh SW, Mehta JP, McGettigan PA, Browne JA, Forde N, Alibrahim RM, Mulligan FJ, Loftus B, Crowe MA, Matthews D, Diskin M, Mihm M, Evans AC. 2012. Effect of the metabolic environment at key stages of follicle development in cattle: focus on steroid biosynthesis. Physiol. Genomics. 44:504-517.   DOI
32 Soberman RJ, Christmas P. 2003. "The organization and consequences of eicosanoid signaling". J. Clin. Invest. 111:1107-1113.   DOI
33 Veshkini A, Asadi H, Khadem AA, Mohammadi-Sangcheshmeh A, Khazabi S, Aminafshar M, Deldar H, Soleimani M, Cinar MU. 2015. Effect of Linolenic acid during in vitro maturation of ovine oocytes: embryonic developmental potential and mRNA abundances of genes involved in apoptosis. J. Assist. Reprod. Genet. 32:653-659.   DOI
34 Viggiano JM, Herrero MB, Cebral E, Boquet MG, de Gimeno MF. 1995. PG synthesis by cumulus-oocyte complexes: effects on in vitro fertilization in mice. PGs Leukot Essent Fatty Acids. 53:261-265.   DOI
35 Wang Y, Botolin D, Christian B, Busik J, Xu J, Jump DB. 2005. Tissue-specific, nutritional, and developmental regulation of rat fatty acid elongases. J. Lipid Res. 46:706-715.   DOI
36 Wiktorowska-Owczarek A, Berezinska M, Nowak JZ. 2015. PUFAs: Structures, Metabolism and Functions. Adv. Clin. Exp. Med. 24:931-941.   DOI
37 Yamashita Y, Shimada M, Okazaki T, Maeda T, Terada T. 2003. Production of progesterone from de novo-synthesized cholesterol in cumulus cells and its physiological role during meiotic resumption of porcine oocytes. Biol. Reprod. 68:1193-1198.   DOI
38 Yoshioka K, Suzuki C, Tanaka A, Anas IM, Iwamura S. 2002. Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol. Reprod. 66:112-119.   DOI