Browse > Article
http://dx.doi.org/10.12749/RDB.2016.40.2.15

A Role of Unsaturated Fatty Acid in Animal Reproductive Cells and Biology  

Hwangbo, Yong (College of Animal Life Sciences, Kangwon National University)
Kim, Hwa-Young (College of Animal Life Sciences, Kangwon National University)
Lee, Yu-Rim (College of Animal Life Sciences, Kangwon National University)
Lee, Seung Tae (College of Animal Life Sciences, Kangwon National University)
Lee, EunSong (College of Veterinary Medicine, Kangwon National University)
Cheong, Hee-Tae (College of Veterinary Medicine, Kangwon National University)
Yang, Boo-Keun (College of Animal Life Sciences, Kangwon National University)
Park, Choon-Keun (College of Animal Life Sciences, Kangwon National University)
Publication Information
Abstract
As a one of unsaturated fatty acid, polyunsaturated fatty acids (PUFAs) have multiple actions: as precursor of prostaglandins (PGs), steroid hormone synthesis and energy production in animal reproduction. PUFAs, which include omega-3 (n-3) and omega-6 (n-6), are derived from the diet and changed by diet, species, breed and season. The plasma membrane of spermatozoa in mammals contain various PUFAs. These composition of PUFAs regulate the membrane fluidity and cause lipid peroxidation via generation of reactive oxygen species (ROS). Induced lipid peroxidation by ROS decreased viability and motility of spermatozoa, and it is reduced by addition of antioxidant and low concentration of PUFAs. Because oocytes of animal have a high lipid components, process of oocyte maturation and embryo development are influenced by PUFAs. In in vitro study, oocyte maturation, embryo development, intracellular cAMP and MAPK activity were increased by treatment of n-3 ${\alpha}$-linolenic acid (ALA) during maturation, whereas n-6 linoleic acid (LA) negatively influenced. Also, inhibition of fatty acid metabolism in oocyte influenced blastocyst formation of cattle. PGs are synthesized from PUFAs and various PUFAs influence PGs via regulation of PG-endoperoxide synthase (PTGS). Steroid hormone synthesis from cholesterol is regulated by expression of steroid acute regulator (StAR) protein and mRNA. Exogenous n-3 and n-6 PUFAs altered sex hormone in animal through stimulate or inhibit StAR activity. Because PUFAs altered PG and steroid hormone synthesis, follicular development was influenced by PUFAs. This effect of unsaturated fatty acid could provide information for improvement of reproductive ability in animals.
Keywords
Unsaturated fatty acid; Reproductive biology; Sperm; Oocyte; Animals;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Stocco DM, Wang X, Jo Y, Manna PR (2005): Multiple signaling pathways regulating steroidogenesis and steroidogenic acute regulatory protein expression: more complicated than we thought. Mol Endocrinol 19:2647-2659.   DOI
2 Sturmey RG, Reis A, Leese HJ, McEvoy TG (2009): Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod Dom Anim 44(s3):50-58.   DOI
3 Sturmey RG, Reis A, Leese HJ, McEvoy TG (2009): Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod Domest Anim 44(Suppl. 3):50-58.   DOI
4 Sutton-McDowall ML, Feil D, Robker RL, Thompsona JG, Dunning KR (2012): Utilization of endogenous fatty acid stores for energy production in bovine preimplantation embryos. Theriogenology 77: 1632-1641.   DOI
5 Tuncer PB, Bucak MN, Buyukleblebici S, Sariozkan S, Yeni D, Eken A, Akalin PP, Kinet H, Avdatek F, Fidan AF, Gundogan M (2010): The effect of cysteine and glutathione on sperm and oxidative stress parameters of post-thawed bull semen. Cryobiology 61:303-307.   DOI
6 Sanocka D, Miesel R, Jedrzejczak P, Chelmonska-Soyta AC, Kurpisz M (1997): Effect of reactive oxygen species and the activity of antioxidant systems on human semen; association with male infertility. Int J Androl 20:255-264.   DOI
7 Veshkini AA, Khadem AA, Soleimani M, Jahanbin R, Salehi M, Alamouti AA, Salehi A, Schellander K, Hoelker M, Mohammadi-Sangcheshmeh A (2012): Exogenous linolenic acid in oocyte maturation media promotes nuclear maturation and parthenogenetic preimplantation embryonic development in the goat. Reprod Fertil Dev 25:280.
8 Waclawik A, Jabbour HN, Blitek A, Ziecik AJ (2009): Estradiol-$17{\beta}$, prostaglandin E2 (PGE2), and the PGE2 receptor are involved in PGE2 positive feedback loop in the porcine endometrium. Endocrinology 150(8):3823-3832.   DOI
9 Wai-Sum O, Chen H, Chow PH (2006): Male genital tract antioxidant enzymes-their ability to preserve sperm DNA integrity. Mol Cell Endocrinol 250: 80-83.   DOI
10 Wang X, Walsh LP, Reinhart AJ, Stocco DM (2000): The role of arachidonic acid in steroidogenesis and steroidogenic acute regulatory (StAR) gene and protein expression. J Biol Chem 275:20204-9.   DOI
11 Wang XJ, Dyson MT, Jo Y, Eubank DW, Stocco DM (2003): Involvement of 5-lipoxygenase metabolites of arachidonic acid in cyclic AMP-stimulated steroidogenesis and steroidogenic acute regulatory protein gene expression. J Steroid Biochem Mol Biol 85:159-166.   DOI
12 Waterhouse KE, Hofmo PO, Tverdal A, Miller Jr RR (2006): Within and breed differences in freezing tolerance and plasma membrane fatty acid composition of boar sperm. Reproduction 131:887-894.   DOI
13 Wathes DC, Abayasekara DR, Aitken RJ (2007): Polyunsaturated fatty acids in male and female reproduction. Biol Reprod 77:190-201.
14 Wathes DC, Cheng Z, Marei W, Fouladi-Nashta A (2013): Polyunsaturated acids and fertility in female mammals: an update. CAB Reviews 8(041):1-14.
15 Witt PM, Christensen JH, Ewertz M, Aardestrup IV, Schmidt EB (2010): The incorporation of marine n-3 PUFA into platelets and adipose tissue in pre- and postmenopausal women: a randomised, double- blind, placebo-controlled trial. Brit J Nutr 104:318-325.   DOI
16 Zeron Y, Ocheretny A, Kedar O, Borochov A, Sklan D, Arav A (2001): Seasonal changes in bovine fertility: relation to developmental competence of oocytes, membrane properties and fatty acid composition of follicles. Reproduction 121:447-454.   DOI
17 Wonnacott KE, Kwong WY, Hughes J, Salter AM, Lea RG, Garnsworthy PC, Sinclair KD (2010): Dietary omega-3 and -6 polyunsaturated fatty acids affect the composition and development of sheep granulosa cells, oocytes and embryos. Reproduction 139: 57-69.   DOI
18 Yi D, Zeng S, Guo Y (2012): A diet rich in n-3 polyunsaturated fatty acids reduced prostaglandin biosynthesis, ovulation rate, and litter size in mice. Theriogenology 78:28-38.   DOI
19 Zachut M, Arieli A, Moallem U (2011): Incorporation of dietary n-3 fatty acids into ovarian compartments in dairy cows and the effects on hormonal and behavioral patterns around estrus. Reproduction 141:833-840.   DOI
20 Zhang XG, Li H, Wang L, Hao YY, Liang GD, Ma YH, Yang GS, Hu JH (2016): The effect of different levels of superoxide dismutase in Modena on boar semen quality during liquid preservation at $17^{\circ}C$. Anim Sci J.
21 Broughton KS, Bayes J, Culver B (2010): High $\alpha$-linolenic acid and fish oil ingestion promotes ovulation to the same extent in rats. Nutr Res 30:731-738.   DOI
22 Abayasekara DRE, Barton LM, Wathes DC (2009): Polyunsaturated fatty acids: effects on steroid hormone biosynthesis. Chapter 26. In: Watson RR, editors. Fatty Acids in Health Promotion and Disease Prevention. Published by AOCS Press, Urbana, IL, USA pp. 707-734.
23 Aitken RJ, Wingate JK, De Iuliis GN, Koppers AJ, McLaughlin EA (2006): Cis-unsaturated fatty acids stimulate reactive oxygen species generation and lipid peroxidation in human spermatozoa. J Clin Endocrinol Metab 91:4154-4163.   DOI
24 Algriany O, Vos PLAM, Sirard MA, Dieleman SJ (2007): Switch in the expression of genes involved in lipid metabolism for in vivo matured bovine oocytes and blastocysts. Reprod Fertil Dev 19:244.
25 Alvarez JG, Storey BT (1995): Differential incorporation of fatty acids into and peroxidative loss of fatty acids from phospholipids of human spermatozoa. Mol Reprod Dev 42:334-336.   DOI
26 Arosh JA, Banu SK, Chapdelaine P, Emond V, Kim JJ, MacLaren LA, Fortier MA (2003): Molecular cloning and characterization of bovine prostaglandin E2 receptors EP2 and EP4: expression and regulation in endometrium and myometrium during the estrous cycle and early pregnancy. Endocrinology 144(7):3076-3091.   DOI
27 Arosh, JA, Parent J, Chapdelaine P, Sirois J, Fortier MA (2002): Expression of cyclooxygenases 1 and 2 and prostaglandin E synthase in bovine endometrial tissue during the estrous cycle. Biol Reprod 67(1): 161-169.   DOI
28 Bilby TR, Block J, Do Amaral BC, Sa Filho O, Silvestre FT, Hansen PJ, Staples CR, Thatcher WW (2006): Effects of dietary unsaturated fatty acids on oocyte quality and follicular development in lactating dairy cows in summer. J Dairy Sci 89(10):3891-3903.   DOI
29 Broughton KS, Hahn B, Ross E (2009a): Docosahexaenoic acid and eicosapentaenoic acid affect ovarian prostaglandin levels differently in rats. Nutr Res 29: 510-518.   DOI
30 Broughton KS, Rule DC, Ye Y, Zhang X, Driscoll M, Culver B (2009b): Dietary omega-3 fatty acids differentially influence ova release and ovarian cyclooxygenase-1 and cyclooxygenase-2 expression in rats. Nutr Res 29:197-205.   DOI
31 Burdge G (2004): Alpha-linolenic acid metabolism in men and women: nutritional and biological implications. Curr Opin Clin Nutr 7:137-144.   DOI
32 Calder PC (2015): Functional roles of fatty acids and their effects on human health. Jpen-Parenter Enter 39(1 suppl):18S-32S.   DOI
33 Cheng Z, Elmes M, Kirkup SE, Abayasekara DRE, Wathes DC (2004): Alteration of prostaglandin production and agonist responsiveness by n-6 polyunsaturated fatty acids in endometrial cells from late gestational ewes. J Endocrinol 182:249-256.   DOI
34 Cao W, Ma Z, Rasenick MM, Yeh S, Yu J (2012): N-3 poly-unsaturated fatty acids shift estrogen signaling to inhibit human breast cancer cell growth. PLoS ONE 7:e52838.   DOI
35 Castaneda CA, Kaye P, Pantaleon M, Phillips N, Norman S, Fry R, Michael JD (2013): Lipid content, active mitochondria and brilliant cresyl blue staining in bovine oocytes. Theriogenology 79:417-422.   DOI
36 Cheng Z, Abayasekara DRE, Wathes DC (2005): The effect of supplementation with n-6 polyunsaturated fatty acids on 1-, 2-and 3-series prostaglandin F production by ovine uterine epithelial cells. BBA-MOL CELL BIOL 1736(2):128-135.
37 Cheng Z, Robinson RS, Pushpakumara PGA, Mansbridge RJ, Wathes DC (2001): Effect of dietary polyunsaturated fatty acids on uterine prostaglandin synthesis in the cow. J Endocrinol 171:463-473.   DOI
38 Childs CE, Romeu-Nadal M, Burdge GC, Calder PC (2008): Gender differences in the n-3 fatty acid content of tissues. P Nutr Soc 67:19-27.   DOI
39 Collado-Fernandez E, Picton HM, Dumollard R (2012): Metabolism throughout follicle and oocyte development in mammals. Int J Dev Biol 56:799-808.   DOI
40 Coull GD, Speake BK, Staines ME, Broadbent PJ, McEvoy TG (1998): Lipid and fatty acid composition of zona-intact sheep oocytes. Theriogenology 49(1):179.   DOI
41 Coyne GS, Kenny DA, Childs S, Sreenan JM, Waters SM (2008): Dietary n-3 polyunsaturated fatty acids alter the expression of genes involved in prostaglandin biosynthesis in the bovine uterus. Theriogenology 70(5):772-782.   DOI
42 Fouladi-Nashta AA, Gutierrez CG, Gong JG, Garnsworthy PC, Webb R (2007): Impact of dietary fatty acids on oocyte quality and development in lactating dairy cows. Biol Reprod 77:9-17.
43 Dacheux JL, Belghazi M, Lanson Y, Dacheux F (2006): Human epididymal secretome and proteome. Mol Cell Endocrinol 250:36-42.   DOI
44 Drevet JR (2006): The antioxidant glutathione peroxidase family and spermatozoa: a complex story. Mol Cell Endocrinol 250:70-79.   DOI
45 Ferguson EM, Leese HJ (2006): A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development. Mol Reprod Dev 73:1195-1201.   DOI
46 Fouladi-Nashta AA, Wonnacott KE, Gutierrez CG, Gong JG, Sinclair KD, Garnsworthy PC, Webb R (2009): Oocyte quality in lactating dairy cows fed on high levels of n-3 and n-6 fatty acids. Reproduction 138: 771-781.   DOI
47 Gomez E, Buckingham DW, Brindle J, Lanzafame F, Irvine DS, Aitken RJ (1996): Development of an image analysis system to monitor the retention of residual cytoplasm by human spermatozoa: correlation with biochemical markers of the cytoplasmic space, oxidative stress, and sperm function. J Androl 17:276-287.
48 Hammiche F, Vujkovic M, Wijburg W, de Vries JH, Macklon NS, Laven JS, Steegers-Theunissen RP (2011): Increased preconception omega-3 polyunsaturated fatty acid intake improves embryo morphology. Fertil Steril 95:1820-1823.   DOI
49 Hansel W, Alila HW, Dowd JP, Yang XZ (1987): Control of steroidogenesis in small and large bovine luteal cells. Aust J Biol Sci 40:331-347.   DOI
50 Herath S, Lilly ST, Fischer DP, Williams EJ, Dobson H, Bryant CE, Sheldon IM (2009): Bacterial lipopolysaccharide induces an endocrine switch from prostaglandin $F_2$ $\alpha$ to prostaglandin E2 in bovine endometrium. Endocrinology 150(4):1912-1920.   DOI
51 Homa ST, Brown CA (1992): Changes in linoleic acid during follicular development and inhibition of spontaneous breakdown of germinal vesicles in cumulus-free bovine oocytes. J Reprod Fertil 94(1):153-160.   DOI
52 Hossain MDS, Tareq LMA, Hammano KI, Tsujji H (2007): Effect of fatty acids on boar sperm motility, viability and acrosome reaction. Reprod Med Biol 6(4):235-239.   DOI
53 Hughes J, Kwong WY, Li D, Salter AM, Lea RG, Sinclair KD (2011): Effects of omega-3 and -6 polyunsaturated fatty acids on ovine follicular cell steroidogenesis, embryo development and molecular markers of fatty acid metabolism. Reproduction 141: 105-18.   DOI
54 Kaka A, Wahid H, Rosnina Y, Yimer N, Khumran AM, Behan AA, Ebrahimi M (2015): Alpha-linolenic acid supplementation in tris extender can improve frozen-thawed bull semen quality. Reprod Dom Anim 50:29-33.   DOI
55 Kasimanickam R, Pelzer KD, Kasimanickam V, Swecker WS, Thatcher CD (2006): Association of classical semen parameters, sperm DNA fragmentation index, lipid peroxidation and antioxidant enzymatic activity of semen in ram-lambs. Theriogenology 65: 1407-1421.   DOI
56 Kim JY, Kinoshita M, Ohnishi M, Fukui Y (2001): Lipid and fatty acid analysis of fresh and frozenthawed immature and in vitro matured bovine oocytes. Reproduction 122:131-138.   DOI
57 Lewis GS (2003): Steroidal regulation of uterine resistance to bacterial infection in livestock. Reprod Biol Endocrin 1:117.   DOI
58 Marei WF, Wathes DC, Fouladi-Nashta AA (2010): Impact of linoleic acid on bovine oocyte maturation and embryo development. Reproduction 139:979-988.   DOI
59 Maldjian A, Pizzi F, Gliozzi T, Cerolini S, Penny P, Noble R (2005): Changes in sperm quality and lipid composition during cryopreservation of boar semen. Theriogenology 63:411-421.   DOI
60 Marei WF, Wathes DC, Fouladi-Nashta AA (2009): Impact of linolenic acid on bovine oocyte maturation and embryo development. Biol Reprod 81:1064-1072.   DOI
61 Marei WF, Wathes DC, Fouladi-Nashta AA (2012): Differential effects of linoleic and alpha-linolenic fatty acids on spatial and temporal mitochondrial distribution and activity in bovine oocytes. Reprod Fertil Dev 24:679-690.   DOI
62 Mattos R, Staples CR, Thatcher WW (2000): Effects of dietary fatty acids on reproduction in ruminants. Rev Reprod 5:38-45.   DOI
63 McEvoy TG, Coull GD, Broadbent PJ, Hutchinson JS, Speake BK (2000): Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J Reprod Fertil 118:163-170.
64 McKeegan PJ, Sturmey RG (2011): The role of fatty acids in oocyte and early embryo development. Reproduction, Fertility and Development 24:59-67.
65 Murakami K, Chan SY, Routtenberg A (1986): Protein kinase C activation by cis-fatty acid in the absence of $Ca^{2+}$ and phospholipids. J Biol Chem 261 (33):15424-15429.
66 Nagashima H, Kashiwazaki N, Ashman R, Grupen C, Seamark RF, Nottle M (1994): Recent advances in cryopreservation of porcine embryos. Theriogenology 41(1):113-118.   DOI
67 Needleman P, Turk J, Kakshik BA, Morrison AR, Lefkowith JB (1986): Arachidonic acid metabolism. Ann Rev Biochem 45:487-510.
68 Patel FA, Funder JW, Challis JR (2003): Mechanism of cortisol/progesterone antagonism in the regulation of 15-hydroxyprostaglandin dehydrogenase activity and messenger ribonucleic acid levels in human chorion and placental trophoblast cells at term. J Clin Endocr Metab 88:2922-2933.   DOI
69 Ollero M, Gil-Guzman E, Lopez MC, Sharma RK, Agarwal A, Larson K, Evenson D, Thomas AJ, Alvarez JG (2001): Characterization of subsets of human spermatozoa at different stages of maturation: implications in the diagnosis and treatment of male infertility. Hum Reprod 16:1912-1921.   DOI
70 Ollero M, Powers RD, Alvarez JG (2000): Variation of docosahexaenoic acid content in subsets of human spermatozoa at different stages of maturation: implications for sperm lipoperoxidative damage. Mol Reprod Dev 55:326-334.   DOI
71 Poulos A, Sharp P, Johnson D, White I, Fellenberg A (1986): The occurrence of polyenoic fatty acids with greater than 22 carbon atoms in mammalian spermatozoa. Biochem J 240:891-895.   DOI
72 Poyser NL (1995): The control of prostaglandin production by the endometrium in relation to luteolysis and menstruation. Prostag Leukotr Ess 53:147-195.   DOI
73 Robinson RS, Pushpakumara PG, Cheng Z, Peters AR, Abayasekara DR, Wathes DC (2002): Effects of dietary polyunsaturated fatty acids on ovarian and uterine function in lactating dairy cows. Reproduction 124(1):119-131.   DOI
74 Santos JEP, Bilby TR, Thatcher WW, Staples CR, Silvestre FT (2008): Long chain fatty acids of diet as factors influencing reproduction in cattle. Reprod Domest Anim 43(suppl 2):23-30.   DOI
75 Songsasen N (2012): Energy metabolism regulating mammalian oocyte maturation. In: Swan A, ed. Meiosis - Molecular Mechanisms and Cytogenetic Diversity. InTech; pp. 173-186.