Numbers of Follicles, Pregnancy, Expression of Reactive Oxygen Species (ROS), and Ovarian Genes in Sheep Treated with Vitamin E, L-Carnitine, and Fish Oil
Abstract
This study was performed to evaluate the effects of vitamin E, L-carnitine, and fish oil on the numbers of follicles, pregnancy, Reactive Oxygen Species (ROS) expression, and expression of several ovarian genes in sheep. For this purpose, 256 sheep were randomly divided into eight experimental groups. They were given a diet supplemented with vitamin E, L-carnitine, and fish oil alone and in combination. FBS, estradiol levels, size of the follicles, and pregnancy rate were observed. Expressions of Superoxide Dismutase 1 (SOD1), Superoxide Dismutase 2 (SOD2), Transforming Growth Factor –β (TGF-β), and Peroxisome Proliferator-Activated Gamma Receptor (PPAR-γ) genes were measured using Reverse Transcription-Polymerase Chain Reaction (RT-PCR), and ROS was measured using fluorescence microscope. At the time of mating and pregnancy, the highest number of follicles and pregnant ewes were observed in the groups supplemented with fish oil and antioxidants (p<0.01). The lowest numbers of follicles and pregnancy was observed in the group supplemented with fish oil alone (p<0.01). The highest expressions of SOD1 and TGF-β genes (p<0.01) as well as SOD2 and PPAR-γ (p<0.05) were observed in the group of concomitant use of fish oil with antioxidants. The highest amount of ROS was found in fish oil group (p<0.01), and the lowest was found in the groups supplemented with fish oil and antioxidant (p<0.01). The use of fish oil along with vitamin E and L-carnitine improved follicle function and increased pregnancy rate by reducing ROS in ewes’ ovaries as well as increasing the expression of SOD1, SOD2, TGF-βRI, and PPAR-γ genes. The use of fish oil along with antioxidants increases follicles and improves fertility in sheep.
References
Adeoye, O., J. Olawumi, A. Opeyemi, & O. Christiania. 2018. Review on the role of glutathione on oxidative stress and infertility. JBRA Assist. Reprod. 22:61-66. https://doi.org/10.5935/1518-0557.20180003
Alemi, M., F. Samadi, & S. Samadi. 2014. Effect of artichoke (Cynara scolymus L.) leaf powder and vitamin E on performance and some blood parameters of meat type Japanese quail. Anim. Prod. 16:147-155.
Ali, A., D. R. Derar, & M. Alshahed. 2019. Management strategies, reproductive performance and causes of infertility in sheep flocks in the central region of Saudi Arabia. Trop. Anim. Health Prod. 52:1-7. https://doi.org/10.1007/s11250-019-02182-9
Assan, N. 2020. Weaning age/time based model influencing performance in goats and sheep meat production. Agricultural Advances 9:537-544.
Attaran, M., E. Pasqualotto, T. Falcone, J. M. Goldberg, K. F. Miller, A. Agarwal, & R. K. Sharma. 2000. The effect of follicular fluid reactive oxygen species on the outcome of in vitro fertilization. Int. J. Fertil. Womens Med. 45:314-320.
Blitek, A. & M. Szymanska. 2019. Regulation of expression and role of peroxisome proliferator-activated receptors (PPARs) in luminal epithelial and stromal cells of the porcine endometrium. Theriogenology 127:88-101. https://doi.org/10.1016/j.theriogenology.2019.01.002
Cam, K., F. Simsek, M. Yuksel, L. Turker, G. Haklar, S. Yalcin, & A. Akdas. 2004. The role of reactive oxygen species and apoptosis in the pathogenesis of varicocele in a rat model and efficiency of vitamin E treatment. Int. J. Androl. 27:228-233. https://doi.org/10.1111/j.1365-2605.2004.00476.x
Cui, Y., K. Miyoshi, E. Claudio, U. K. Siebenlist, F. J. Gonzalez, J. Flaws, K. U. Wagner, & L. Hennighausen. 2002. Loss of the peroxisome proliferation-activated receptor gamma (PPARγ) does not affect mammary development and propensity for tumor formation but leads to reduced fertility. J. Biol. Chem. 277:17830-17835. https://doi.org/10.1074/jbc.M200186200
De Pascale, M. C., A. M. Bassi, V. Patrone, L. Villacorta, A. Azzi, & J. M. Zingg. 2006. Increased expression of transglutaminase-1 and PPARγ after vitamin E treatment in human keratinocytes. Arch. Biochem. Biophys. 447:97-106. https://doi.org/10.1016/j.abb.2006.02.002
Ďuračková, Z. 2010. Some current insights into oxidative stress. Physiol. Res. 59:459-469. https://doi.org/10.33549/physiolres.931844
Durmuş, M. 2018. Fish oil for human health: Omega-3 fatty acid profiles of marine seafood species. Food Sci. Technol. 39:454-461. https://doi.org/10.1590/fst.21318
Elizur, S. E., O. Lebovitz, R. Orvieto, J. Dor, & T. Zan-Bar. 2014. Reactive oxygen species in follicular fluid may serve as biochemical markers to determine ovarian aging and follicular metabolic age. J. Gynaecol. Endocrinol. 30:705-707. https://doi.org/10.3109/09513590.2014.924100
Ferreira, E. M., A.V. Pires, I. Susin, R. S. Gentil, S. Gilaverte, M. D. O. M. Parente, M. V. Biehl, & C. V. D. M. Ribeiro. 2014. Lamb performance, milk production and composition from ewes supplemented with soybean oil partially replaced by fish oil blend. Livest. Sci. 163:51-61. https://doi.org/10.1016/j.livsci.2014.02.009
Foroozandeh, A. D., H. R. Amini, G. R. Ghalamkari, M. Shahzeydi, & S. M. Nasrollahi. 2014. The effect of fat type and l-carnitine administration on growth, feed digestibility and blood metabolites of growing Afshari lambs. Livest. Sci. 164:67-71. https://doi.org/10.1016/j.livsci.2014.03.019
Galloway, S. M., K. P. McNatty, L. M. Cambridge, M. P. Laitinen, J. L. Juengel, T. S. Jokiranta, R. J. McLaren, K. Luiro, K. G. Dodds, G. W. Montgomery, & A. E. Beattie. 2000. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat. Genet. 25:279-283. https://doi.org/10.1038/77033
Ghasemzadeh, A., L. Farzadi, A. Khaki, & S. K. Ahmadi. 2013. Effect of Allium cepa seeds ethanolic extract on experimental polycystic ovary syndrome (PCOS) apoptosis induced by estradiol-valerate. Life Sci. J. 10:170-175.
Gill, S. S., N. A. Anjum, R. Gill, S. Yadav, M. Hasanuzzaman, M. Fujita, P. Mishra, S. C. Sabat, & N. Tuteja. 2015. Superoxide dismutase—mentor of abiotic stress tolerance in crop plants. Environ. Sci. Poullt. Res. 22:10375-10394. https://doi.org/10.1007/s11356-015-4532-5
Gulcin, I., M. E. Buyukokuroglu, M. Oktay, & O. I. Kufrevioglu. 2002. On the in vitro antioxidative properties of melatonin. J. Pineal Res. 33:167-171. https://doi.org/10.1034/j.1600-079X.2002.20920.x
Hao, F., X. Wang, & J. Chen. 2006. Involvement of plasma-membrane NADPH oxidase in nickel-induced oxidative stress in roots of wheat seedlings. Plant Sci. 170:151-158. https://doi.org/10.1016/j.plantsci.2005.08.014
Hara, S., T. Takahashi, M. Amita, K. Matsuo, H. Igarashi, & H. Kurachi. 2013. Pioglitazone counteracts the tumor necrosis factor-α inhibition of follicle-stimulating hormone-induced follicular development and estradiol production in an in vitro mouse preantral follicle culture system. J. Ovarian. Res. 6:1-8. https://doi.org/10.1186/1757-2215-6-69
Heinecke, J. W. 2002. Oxidized amino acids: Culprits in human atherosclerosis and indicators of oxidative stress. Free Radic. Biol. Med. 32:1090-1101. https://doi.org/10.1016/S0891-5849(02)00792-X
Hill, T. M., H. G. Bateman II, J. M. Aldrich, & R. L. Schlotterbeck. 2009. Effects of changing the essential and functional fatty acid intake of dairy calves. J. Dairy Sci. 92:670-676. https://doi.org/10.3168/jds.2008-1368
Huang, W. J., X. I. A. Zhang, & W. W. Chen. 2016. Role of oxidative stress in Alzheimer’s disease. Biomed. Rep. 4:519-522. https://doi.org/10.3892/br.2016.630
Ighodaro, O. M. & O. A. Akinloye. 2018. First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alexandria J. Med. 54:287-293. https://doi.org/10.1016/j.ajme.2017.09.001
Ishikawa, H., A. Takaki, R. Tsuzaki, T. Yasunaka, K. Koike, Y. Shimomura, H. Seki, H. Matsushita, Y. Miyake, F. Ikeda, & H. Shiraha. 2014. L-carnitine prevents progression of non-alcoholic steatohepatitis in a mouse model with upregulation of mitochondrial pathway. PLoS ONE 9:e100627. https://doi.org/10.1371/journal.pone.0100627
Jia, Y., Q. Jing, H. Niu, & B. Huang. 2017. Ameliorative effect of vitamin E on hepatic oxidative stress and hypoimmunity induced by high-fat diet in turbot (Scophthalmus maximus). Fish Shellfish. Immunol. 67:634-642. https://doi.org/10.1016/j.fsi.2017.06.056
Jin, M., T. Pan, X. Cheng, T. T. Zhu, P. Sun, F. Zhou, X. Ding, & Q. Zhou. 2019. Effects of supplemental dietary L-carnitine and bile acids on growth performance, antioxidant and immune ability, histopathological changes and inflammatory response in juvenile black seabream (Acanthopagrus schlegelii) fed high-fat diet. Aquaculture 504:199-209. https://doi.org/10.1016/j.aquaculture.2019.01.063
Kala, M. 2017. Role of stress and stress hormones on ovulation and implantation in mice involvement of adrenals. Institute of Pharmacy, Nirma University. http://hdl.handle.net/10603/188038
Kehrer, J. P. & L. O. Klotz. 2015. Free radicals and related reactive species as mediators of tissue injury and disease: Implications for health. Crit. Rev. Toxicol. 45:765-798. https://doi.org/10.3109/10408444.2015.1074159
Kielian, T. & P. D. Drew. 2003. Effects of peroxisome proliferator‐activated receptor‐γ agonists on central nervous system inflammation. J. Neurosci. Res. 71:315-325. https://doi.org/10.1002/jnr.10501
Kim, J. C., Y. H. Lee, M. K. Yu, N. H. Lee, J. D. Park, G. Bhattarai, & H. K. Yi. 2012. Anti-inflammatory mechanism of PPARγ on LPS-induced pulp cells: Role of the ROS removal activity. Arch. Oral. Biol. 57:392-400. https://doi.org/10.1016/j.archoralbio.2011.09.009
Kumaran, S., K. S. Panneerselvam, S. Shila, K. Sivarajan, & C. Panneerselvam. 2005. Age-associated deficit of mitochondrial oxidative phosphorylation in skeletal muscle: Role of carnitine and lipoic acid. Mol. Cell. Biochem. 280:83-89. https://doi.org/10.1007/s11010-005-8234-z
Lee, G. Y. & S. N. Han. 2018. The role of vitamin E in immunity. Nutrients. 10:1614. https://doi.org/10.3390/nu10111614
Lee, Y. H., F. Y. Cheng, H. W. Chiu, J. C. Tsai, C. Y. Fang, C. W. Chen, & Y. J. Wang. 2014. Cytotoxicity, oxidative stress, apoptosis and the autophagic effects of silver nanoparticles in mouse embryonic fibroblasts. Biomaterials 35:4706-4715. https://doi.org/10.1016/j.biomaterials.2014.02.021
Lewis, E. D., S. N. Meydani, & D. Wu. 2019. Regulatory role of vitamin E in the immune system and inflammation. IUBMB Life. 71:487-494. https://doi.org/10.1002/iub.1976
Li, J. & X. Y. Yu. 2012. Effects of exogenous carnitine on function of respiratory chain and antioxidant capacity in mitochondria of myocardium after exhaustive running in rats. Zhongguo Ying Yong Sheng Li Xue Za Zhi. 28:405-409.
Li, Z., X. Xu, X. Leng, M. He, J. Wang, S. Cheng, & H. Wu. 2017. Roles of reactive oxygen species in cell signaling pathways and immune responses to viral infections. Arch. Virol. 162:603-610. https://doi.org/10.1007/s00705-016-3130-2
Livak, K. J. & T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402-408. https://doi.org/10.1006/meth.2001.1262
Lu, J., Z. Wang, J. Cao, Y. Chen, & Y. Dong. 2018. A novel and compact review on the role of oxidative stress in female reproduction. Reprod. Biol. Endocrinol. 16:1-18. https://doi.org/10.1186/s12958-018-0391-5
Manickam, V., M. Periyasamy, V. Dhakshinamoorthy, L. Panneerselvam, & E. Perumal. 2017. Recurrent exposure to ferric oxide nanoparticles alters myocardial oxidative stress, apoptosis and necrotic markers in male mice. Chem. Biol. Interact. 278:54-64. https://doi.org/10.1016/j.cbi.2017.10.003
Matsuzawa, A. & H. Ichijo. 2008. Redox control of cell fate by MAP kinase: Physiological roles of ASK1-MAP kinase pathway in stress signaling. Biochim. Biophys. Acta Gen. Subj. 1780:1325-1336. https://doi.org/10.1016/j.bbagen.2007.12.011
McCord, J. M. & I. Fridovich. 1969. Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). Journal Biological Chemistry. 244:6049-6055. https://doi.org/10.1016/S0021-9258(18)63504-5
Minge, C. E., R. L. Robker, & R. J. Norman. 2008. PPAR gamma: Coordinating metabolic and immune contributions to female fertility. PPAR. Res. 2008:243791. https://doi.org/10.1155/2008/243791
Mishra, A., I. J. Reddy, P. S. P. Gupta, & S. Mondal. 2016. l‐carnitine mediated reduction in oxidative stress and alteration in transcript level of antioxidant enzymes in sheep embryos produced in vitro. Reprod. Domest. Anim. 51:311-321. https://doi.org/10.1111/rda.12682
Mishra, A., I. J. Reddy, P. S. P. Gupta, & S. Mondal. 2017. Expression of apoptotic and antioxidant enzyme genes in sheep oocytes and in vitro produced embryos. Anim. Biotechnol. 28:18-25. https://doi.org/10.1080/10495398.2016.1193743
Moallem, U., A. Shafran, M. Zachut, I. Dekel, Y. Portnick, & A. Arieli. 2013. Dietary a-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. https://doi.org/10.1530/REP-13-0244
Monsivais, D., M. M. Matzuk, & S. A. Pangas. 2017. The TGF-β family in the reproductive tract. Col. Spr. Har. Per. Bio. 9:022251. https://doi.org/10.1101/cshperspect.a022251
Mugabe, L. C., A. R. Bagaldo, L. P. Barbosa, F. L. D. Araújo, B. Y. D. S. Oliveira, R. V. M. M. Silva, R. L. Oliveira, & E. E. G. Pinheiro. 2017. Biochemical and seminal parameters of lambs fed palm kernel cake under grazing system. Revista Brasileira de Zootecnia 46:670-677. https://doi.org/10.1590/s1806-92902017000800007
Nateghi, R., A. Alizadeh, Y. J. Ahangari, R. Fathi, & A. Akhlaghi. 2019. Stimulatory effects of fish oil and vitamin E on ovarian function of laying hen. Ital. J. Anim. Sci. 18:636-645. https://doi.org/10.1080/1828051X.2018.1551071
Nehra, D., H. D. Le, E. M. Fallon, S. J. Carlson, D. Woods, Y. A. White, A. H. Pan, L. Guo, S. J. Rodig, J. L. Tilly, & B. R. Rueda. 2012. Prolonging the female reproductive lifespan and improving egg quality with dietary omega‐3 fatty acids. Aging Cell. 11:1046-1054. https://doi.org/10.1111/acel.12006
Olsen, S. F., J. D. Sørensen, N. J. Secher, M. Hedegaard, T. B. Henriksen, H. S. Hansen, & A. Grant. 1992. Randomised controlled trial of effect of fish-oil supplementation on pregnancy duration. Lancet. 339:1003-1007. https://doi.org/10.1016/0140-6736(92)90533-9
Raja-Khan, N., M. Urbanek, R. J. Rodgers, & R. S. Legro. 2014. The role of TGF-β in polycystic ovary syndrome. Reprod. Sci. 21:20-31. https://doi.org/10.1177/1933719113485294
Reuter, S., S. C. Gupta, M. M. Chaturvedi, & B. B. Aggarwal. 2010. Oxidative stress, inflammation, and cancer: How are they linked. Free Radic. Biol. Med. 49:1603-1616. https://doi.org/10.1016/j.freeradbiomed.2010.09.006
Rodrigues, G. Q., M. J. Bertoldo, I. R. Brito, C. M. G. Silva, A. D. Sales, S. V. Castro, N. Duffard, Y. Locatelli, P. Mermillod, C. H. Lobo, & C. C. Campello. 2014. Relative mRNA expression and immunolocalization for transforming growth factor-beta (TGF-β) and their effect on in vitro development of caprine preantral follicles. In Vitro Cell. Dev. Biol. Anim. 50:688-699. https://doi.org/10.1007/s11626-014-9775-9
Rosairo, D., I. Kuyznierewicz, J. Findlay, & A. Drummond. 2008. Transforming growth factor-β: its role in ovarian follicle development. Reproduction 136:799-809. https://doi.org/10.1530/REP-08-0310
Rostamtabar, M., S. Esmaeilzadeh, M. Tourani, A. Rahmani, M. Baee, F. Shirafkan, K. Saleki, S. S. Mirzababayi, S. Ebrahimpour, & H. R. Nouri. 2021. Pathophysiological roles of chronic low‐grade inflammation mediators in polycystic ovary syndrome. J. Cell. Physiol. 236:824-838. https://doi.org/10.1002/jcp.29912
Ruiz-Sanz, J. I., I. Pérez-Ruiz, S. Meijide, M. Ferrando, Z. Larreategui, & M. B. Ruiz-Larrea. 2019. Lower follicular n-3 polyunsaturated fatty acid levels are associated with a better response to ovarian stimulation. J. Assist. Reprod. Genet. 36:473-482. https://doi.org/10.1007/s10815-018-1384-1
Sherratt, S. C., M. Lero, & R. P. Mason. 2020. Are dietary fish oil supplements appropriate for dyslipidemia management? A review of the evidence. Curr. Opin. Lipidol. 31:94-100. https://doi.org/10.1097/MOL.0000000000000665
Shokrzadeh, M., N. Ahangar, M. Zargari, Z. Gilani, A. Shadboorestan, & M. Omidi. 2013. Protective effect of L-carnitine on level of malondialdehyde in diazinon-induced lipid peroxidation in rats. Jou. Maz. Uni. Med. Sci. 22:198-206.
Sun, S., F. Xie, Q. Zhang, Z. Cui, X. Cheng, F. Zhong, K. He, & J. Zhou. 2017. Advanced oxidation protein products induce hepatocyte epithelial–mesenchymal transition via a ROS‐dependent, TGF‐β/Smad signaling pathway. Cell. Biol. Int. 41:842-853. https://doi.org/10.1002/cbin.10792
Sun, W. H., F. Liu, Y. Chen, & Y. C. Zhu. 2012. Hydrogen sulfide decreases the levels of ROS by inhibiting mitochondrial complex IV and increasing SOD activities in cardiomyocytes under ischemia/reperfusion. Biochem. Biophys. Res. Commun. 421:164-169. https://doi.org/10.1016/j.bbrc.2012.03.121
Sung, C. C., Y. C. Hsu, C. C. Chen, Y. F. Lin, & C. C. Wu. 2013. Oxidative stress and nucleic acid oxidation in patients with chronic kidney disease. Oxid. Med. Cell. Longev. 2013:301982. https://doi.org/10.1155/2013/301982
Surai, P. F. 2015. Antioxidant action of carnitine: Molecular mechanisms and practical applications. EC. Vet. Sci. 2:66-84.
Torquato, P., R. Marinelli, D. Bartolini, & F. Galli. 2020. Vitamin E: Nutritional aspects. Mol. Nut. 2020:447-485. Mol. Nutr. https://doi.org/10.1016/B978-0-12-811907-5.00019-1
Vitti, M., G. D. Emidio, M. D. Carlo, G. Carta, A. Antonosante, P. G. Artini, A. Cimini, C. Tatone, & E. Benedetti. 2016. Peroxisome proliferator-activated receptors in female reproduction and fertility. PPAR. Res. 2016:4612306. https://doi.org/10.1155/2016/4612306
Wang, Q. L., J. L. Yuan, Y. Y. Tao, Y. Zhang, P. Liu, & C. H. Liu. 2010. Fuzheng Huayu recipe and vitamin E reverse renal interstitial fibrosis through counteracting TGF-β1-induced epithelial-to-mesenchymal transition. J. Ethnopharmacol. 127:631-640. https://doi.org/10.1016/j.jep.2009.12.011
Wiemer, E. A. 2011. Stressed tumor cell, chemosensitized cancer. Nat. Med. 17:1552-1554. https://doi.org/10.1038/nm.2593
Yang, J., Y. Zhang, X. Xu, J. Li, F. Yuan, S. Bo, J. Qiao, G. Xia, Y. Su, & M. Zhang. 2019. Transforming growth factor-β is involved in maintaining oocyte meiotic arrest by promoting natriuretic peptide type C expression in mouse granulosa cells. Cell Death Dis. 10:558. https://doi.org/10.1038/s41419-019-1797-5
Zarezadeh, R., A. Mehdizadeh, J. L. Leroy, M. Nouri, S. Fayezi, & M. Darabi. 2019. Action mechanisms of n‐3 polyunsaturated fatty acids on the oocyte maturation and developmental competence: Potential advantages and disadvantages. J. Cell. Physiol. 234:1016-1029. https://doi.org/10.1002/jcp.27101
Zhang, X., R. K. Sharma, A. Agarwal, & T. Falcone. 2005. Effect of pentoxifylline in reducing oxidative stress-induced embryotoxicity. J. Assist. Reprod. Genet. 22:415-417.
https://doi.org/10.1007/s10815-005-7202-6
Zhou, S., Y. Ma, J. Yao, A. Zhao, C. Xie, Y. Mi, & C. Zhang. 2021. TGF‐β1‐induced collagen promotes chicken ovarian follicle development via an intercellular cooperative pattern. Cell. Biol. Int. 45:1336-1348. https://doi.org/10.1002/cbin.11580
Alemi, M., F. Samadi, & S. Samadi. 2014. Effect of artichoke (Cynara scolymus L.) leaf powder and vitamin E on performance and some blood parameters of meat type Japanese quail. Anim. Prod. 16:147-155.
Ali, A., D. R. Derar, & M. Alshahed. 2019. Management strategies, reproductive performance and causes of infertility in sheep flocks in the central region of Saudi Arabia. Trop. Anim. Health Prod. 52:1-7. https://doi.org/10.1007/s11250-019-02182-9
Assan, N. 2020. Weaning age/time based model influencing performance in goats and sheep meat production. Agricultural Advances 9:537-544.
Attaran, M., E. Pasqualotto, T. Falcone, J. M. Goldberg, K. F. Miller, A. Agarwal, & R. K. Sharma. 2000. The effect of follicular fluid reactive oxygen species on the outcome of in vitro fertilization. Int. J. Fertil. Womens Med. 45:314-320.
Blitek, A. & M. Szymanska. 2019. Regulation of expression and role of peroxisome proliferator-activated receptors (PPARs) in luminal epithelial and stromal cells of the porcine endometrium. Theriogenology 127:88-101. https://doi.org/10.1016/j.theriogenology.2019.01.002
Cam, K., F. Simsek, M. Yuksel, L. Turker, G. Haklar, S. Yalcin, & A. Akdas. 2004. The role of reactive oxygen species and apoptosis in the pathogenesis of varicocele in a rat model and efficiency of vitamin E treatment. Int. J. Androl. 27:228-233. https://doi.org/10.1111/j.1365-2605.2004.00476.x
Cui, Y., K. Miyoshi, E. Claudio, U. K. Siebenlist, F. J. Gonzalez, J. Flaws, K. U. Wagner, & L. Hennighausen. 2002. Loss of the peroxisome proliferation-activated receptor gamma (PPARγ) does not affect mammary development and propensity for tumor formation but leads to reduced fertility. J. Biol. Chem. 277:17830-17835. https://doi.org/10.1074/jbc.M200186200
De Pascale, M. C., A. M. Bassi, V. Patrone, L. Villacorta, A. Azzi, & J. M. Zingg. 2006. Increased expression of transglutaminase-1 and PPARγ after vitamin E treatment in human keratinocytes. Arch. Biochem. Biophys. 447:97-106. https://doi.org/10.1016/j.abb.2006.02.002
Ďuračková, Z. 2010. Some current insights into oxidative stress. Physiol. Res. 59:459-469. https://doi.org/10.33549/physiolres.931844
Durmuş, M. 2018. Fish oil for human health: Omega-3 fatty acid profiles of marine seafood species. Food Sci. Technol. 39:454-461. https://doi.org/10.1590/fst.21318
Elizur, S. E., O. Lebovitz, R. Orvieto, J. Dor, & T. Zan-Bar. 2014. Reactive oxygen species in follicular fluid may serve as biochemical markers to determine ovarian aging and follicular metabolic age. J. Gynaecol. Endocrinol. 30:705-707. https://doi.org/10.3109/09513590.2014.924100
Ferreira, E. M., A.V. Pires, I. Susin, R. S. Gentil, S. Gilaverte, M. D. O. M. Parente, M. V. Biehl, & C. V. D. M. Ribeiro. 2014. Lamb performance, milk production and composition from ewes supplemented with soybean oil partially replaced by fish oil blend. Livest. Sci. 163:51-61. https://doi.org/10.1016/j.livsci.2014.02.009
Foroozandeh, A. D., H. R. Amini, G. R. Ghalamkari, M. Shahzeydi, & S. M. Nasrollahi. 2014. The effect of fat type and l-carnitine administration on growth, feed digestibility and blood metabolites of growing Afshari lambs. Livest. Sci. 164:67-71. https://doi.org/10.1016/j.livsci.2014.03.019
Galloway, S. M., K. P. McNatty, L. M. Cambridge, M. P. Laitinen, J. L. Juengel, T. S. Jokiranta, R. J. McLaren, K. Luiro, K. G. Dodds, G. W. Montgomery, & A. E. Beattie. 2000. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat. Genet. 25:279-283. https://doi.org/10.1038/77033
Ghasemzadeh, A., L. Farzadi, A. Khaki, & S. K. Ahmadi. 2013. Effect of Allium cepa seeds ethanolic extract on experimental polycystic ovary syndrome (PCOS) apoptosis induced by estradiol-valerate. Life Sci. J. 10:170-175.
Gill, S. S., N. A. Anjum, R. Gill, S. Yadav, M. Hasanuzzaman, M. Fujita, P. Mishra, S. C. Sabat, & N. Tuteja. 2015. Superoxide dismutase—mentor of abiotic stress tolerance in crop plants. Environ. Sci. Poullt. Res. 22:10375-10394. https://doi.org/10.1007/s11356-015-4532-5
Gulcin, I., M. E. Buyukokuroglu, M. Oktay, & O. I. Kufrevioglu. 2002. On the in vitro antioxidative properties of melatonin. J. Pineal Res. 33:167-171. https://doi.org/10.1034/j.1600-079X.2002.20920.x
Hao, F., X. Wang, & J. Chen. 2006. Involvement of plasma-membrane NADPH oxidase in nickel-induced oxidative stress in roots of wheat seedlings. Plant Sci. 170:151-158. https://doi.org/10.1016/j.plantsci.2005.08.014
Hara, S., T. Takahashi, M. Amita, K. Matsuo, H. Igarashi, & H. Kurachi. 2013. Pioglitazone counteracts the tumor necrosis factor-α inhibition of follicle-stimulating hormone-induced follicular development and estradiol production in an in vitro mouse preantral follicle culture system. J. Ovarian. Res. 6:1-8. https://doi.org/10.1186/1757-2215-6-69
Heinecke, J. W. 2002. Oxidized amino acids: Culprits in human atherosclerosis and indicators of oxidative stress. Free Radic. Biol. Med. 32:1090-1101. https://doi.org/10.1016/S0891-5849(02)00792-X
Hill, T. M., H. G. Bateman II, J. M. Aldrich, & R. L. Schlotterbeck. 2009. Effects of changing the essential and functional fatty acid intake of dairy calves. J. Dairy Sci. 92:670-676. https://doi.org/10.3168/jds.2008-1368
Huang, W. J., X. I. A. Zhang, & W. W. Chen. 2016. Role of oxidative stress in Alzheimer’s disease. Biomed. Rep. 4:519-522. https://doi.org/10.3892/br.2016.630
Ighodaro, O. M. & O. A. Akinloye. 2018. First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alexandria J. Med. 54:287-293. https://doi.org/10.1016/j.ajme.2017.09.001
Ishikawa, H., A. Takaki, R. Tsuzaki, T. Yasunaka, K. Koike, Y. Shimomura, H. Seki, H. Matsushita, Y. Miyake, F. Ikeda, & H. Shiraha. 2014. L-carnitine prevents progression of non-alcoholic steatohepatitis in a mouse model with upregulation of mitochondrial pathway. PLoS ONE 9:e100627. https://doi.org/10.1371/journal.pone.0100627
Jia, Y., Q. Jing, H. Niu, & B. Huang. 2017. Ameliorative effect of vitamin E on hepatic oxidative stress and hypoimmunity induced by high-fat diet in turbot (Scophthalmus maximus). Fish Shellfish. Immunol. 67:634-642. https://doi.org/10.1016/j.fsi.2017.06.056
Jin, M., T. Pan, X. Cheng, T. T. Zhu, P. Sun, F. Zhou, X. Ding, & Q. Zhou. 2019. Effects of supplemental dietary L-carnitine and bile acids on growth performance, antioxidant and immune ability, histopathological changes and inflammatory response in juvenile black seabream (Acanthopagrus schlegelii) fed high-fat diet. Aquaculture 504:199-209. https://doi.org/10.1016/j.aquaculture.2019.01.063
Kala, M. 2017. Role of stress and stress hormones on ovulation and implantation in mice involvement of adrenals. Institute of Pharmacy, Nirma University. http://hdl.handle.net/10603/188038
Kehrer, J. P. & L. O. Klotz. 2015. Free radicals and related reactive species as mediators of tissue injury and disease: Implications for health. Crit. Rev. Toxicol. 45:765-798. https://doi.org/10.3109/10408444.2015.1074159
Kielian, T. & P. D. Drew. 2003. Effects of peroxisome proliferator‐activated receptor‐γ agonists on central nervous system inflammation. J. Neurosci. Res. 71:315-325. https://doi.org/10.1002/jnr.10501
Kim, J. C., Y. H. Lee, M. K. Yu, N. H. Lee, J. D. Park, G. Bhattarai, & H. K. Yi. 2012. Anti-inflammatory mechanism of PPARγ on LPS-induced pulp cells: Role of the ROS removal activity. Arch. Oral. Biol. 57:392-400. https://doi.org/10.1016/j.archoralbio.2011.09.009
Kumaran, S., K. S. Panneerselvam, S. Shila, K. Sivarajan, & C. Panneerselvam. 2005. Age-associated deficit of mitochondrial oxidative phosphorylation in skeletal muscle: Role of carnitine and lipoic acid. Mol. Cell. Biochem. 280:83-89. https://doi.org/10.1007/s11010-005-8234-z
Lee, G. Y. & S. N. Han. 2018. The role of vitamin E in immunity. Nutrients. 10:1614. https://doi.org/10.3390/nu10111614
Lee, Y. H., F. Y. Cheng, H. W. Chiu, J. C. Tsai, C. Y. Fang, C. W. Chen, & Y. J. Wang. 2014. Cytotoxicity, oxidative stress, apoptosis and the autophagic effects of silver nanoparticles in mouse embryonic fibroblasts. Biomaterials 35:4706-4715. https://doi.org/10.1016/j.biomaterials.2014.02.021
Lewis, E. D., S. N. Meydani, & D. Wu. 2019. Regulatory role of vitamin E in the immune system and inflammation. IUBMB Life. 71:487-494. https://doi.org/10.1002/iub.1976
Li, J. & X. Y. Yu. 2012. Effects of exogenous carnitine on function of respiratory chain and antioxidant capacity in mitochondria of myocardium after exhaustive running in rats. Zhongguo Ying Yong Sheng Li Xue Za Zhi. 28:405-409.
Li, Z., X. Xu, X. Leng, M. He, J. Wang, S. Cheng, & H. Wu. 2017. Roles of reactive oxygen species in cell signaling pathways and immune responses to viral infections. Arch. Virol. 162:603-610. https://doi.org/10.1007/s00705-016-3130-2
Livak, K. J. & T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402-408. https://doi.org/10.1006/meth.2001.1262
Lu, J., Z. Wang, J. Cao, Y. Chen, & Y. Dong. 2018. A novel and compact review on the role of oxidative stress in female reproduction. Reprod. Biol. Endocrinol. 16:1-18. https://doi.org/10.1186/s12958-018-0391-5
Manickam, V., M. Periyasamy, V. Dhakshinamoorthy, L. Panneerselvam, & E. Perumal. 2017. Recurrent exposure to ferric oxide nanoparticles alters myocardial oxidative stress, apoptosis and necrotic markers in male mice. Chem. Biol. Interact. 278:54-64. https://doi.org/10.1016/j.cbi.2017.10.003
Matsuzawa, A. & H. Ichijo. 2008. Redox control of cell fate by MAP kinase: Physiological roles of ASK1-MAP kinase pathway in stress signaling. Biochim. Biophys. Acta Gen. Subj. 1780:1325-1336. https://doi.org/10.1016/j.bbagen.2007.12.011
McCord, J. M. & I. Fridovich. 1969. Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). Journal Biological Chemistry. 244:6049-6055. https://doi.org/10.1016/S0021-9258(18)63504-5
Minge, C. E., R. L. Robker, & R. J. Norman. 2008. PPAR gamma: Coordinating metabolic and immune contributions to female fertility. PPAR. Res. 2008:243791. https://doi.org/10.1155/2008/243791
Mishra, A., I. J. Reddy, P. S. P. Gupta, & S. Mondal. 2016. l‐carnitine mediated reduction in oxidative stress and alteration in transcript level of antioxidant enzymes in sheep embryos produced in vitro. Reprod. Domest. Anim. 51:311-321. https://doi.org/10.1111/rda.12682
Mishra, A., I. J. Reddy, P. S. P. Gupta, & S. Mondal. 2017. Expression of apoptotic and antioxidant enzyme genes in sheep oocytes and in vitro produced embryos. Anim. Biotechnol. 28:18-25. https://doi.org/10.1080/10495398.2016.1193743
Moallem, U., A. Shafran, M. Zachut, I. Dekel, Y. Portnick, & A. Arieli. 2013. Dietary a-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. https://doi.org/10.1530/REP-13-0244
Monsivais, D., M. M. Matzuk, & S. A. Pangas. 2017. The TGF-β family in the reproductive tract. Col. Spr. Har. Per. Bio. 9:022251. https://doi.org/10.1101/cshperspect.a022251
Mugabe, L. C., A. R. Bagaldo, L. P. Barbosa, F. L. D. Araújo, B. Y. D. S. Oliveira, R. V. M. M. Silva, R. L. Oliveira, & E. E. G. Pinheiro. 2017. Biochemical and seminal parameters of lambs fed palm kernel cake under grazing system. Revista Brasileira de Zootecnia 46:670-677. https://doi.org/10.1590/s1806-92902017000800007
Nateghi, R., A. Alizadeh, Y. J. Ahangari, R. Fathi, & A. Akhlaghi. 2019. Stimulatory effects of fish oil and vitamin E on ovarian function of laying hen. Ital. J. Anim. Sci. 18:636-645. https://doi.org/10.1080/1828051X.2018.1551071
Nehra, D., H. D. Le, E. M. Fallon, S. J. Carlson, D. Woods, Y. A. White, A. H. Pan, L. Guo, S. J. Rodig, J. L. Tilly, & B. R. Rueda. 2012. Prolonging the female reproductive lifespan and improving egg quality with dietary omega‐3 fatty acids. Aging Cell. 11:1046-1054. https://doi.org/10.1111/acel.12006
Olsen, S. F., J. D. Sørensen, N. J. Secher, M. Hedegaard, T. B. Henriksen, H. S. Hansen, & A. Grant. 1992. Randomised controlled trial of effect of fish-oil supplementation on pregnancy duration. Lancet. 339:1003-1007. https://doi.org/10.1016/0140-6736(92)90533-9
Raja-Khan, N., M. Urbanek, R. J. Rodgers, & R. S. Legro. 2014. The role of TGF-β in polycystic ovary syndrome. Reprod. Sci. 21:20-31. https://doi.org/10.1177/1933719113485294
Reuter, S., S. C. Gupta, M. M. Chaturvedi, & B. B. Aggarwal. 2010. Oxidative stress, inflammation, and cancer: How are they linked. Free Radic. Biol. Med. 49:1603-1616. https://doi.org/10.1016/j.freeradbiomed.2010.09.006
Rodrigues, G. Q., M. J. Bertoldo, I. R. Brito, C. M. G. Silva, A. D. Sales, S. V. Castro, N. Duffard, Y. Locatelli, P. Mermillod, C. H. Lobo, & C. C. Campello. 2014. Relative mRNA expression and immunolocalization for transforming growth factor-beta (TGF-β) and their effect on in vitro development of caprine preantral follicles. In Vitro Cell. Dev. Biol. Anim. 50:688-699. https://doi.org/10.1007/s11626-014-9775-9
Rosairo, D., I. Kuyznierewicz, J. Findlay, & A. Drummond. 2008. Transforming growth factor-β: its role in ovarian follicle development. Reproduction 136:799-809. https://doi.org/10.1530/REP-08-0310
Rostamtabar, M., S. Esmaeilzadeh, M. Tourani, A. Rahmani, M. Baee, F. Shirafkan, K. Saleki, S. S. Mirzababayi, S. Ebrahimpour, & H. R. Nouri. 2021. Pathophysiological roles of chronic low‐grade inflammation mediators in polycystic ovary syndrome. J. Cell. Physiol. 236:824-838. https://doi.org/10.1002/jcp.29912
Ruiz-Sanz, J. I., I. Pérez-Ruiz, S. Meijide, M. Ferrando, Z. Larreategui, & M. B. Ruiz-Larrea. 2019. Lower follicular n-3 polyunsaturated fatty acid levels are associated with a better response to ovarian stimulation. J. Assist. Reprod. Genet. 36:473-482. https://doi.org/10.1007/s10815-018-1384-1
Sherratt, S. C., M. Lero, & R. P. Mason. 2020. Are dietary fish oil supplements appropriate for dyslipidemia management? A review of the evidence. Curr. Opin. Lipidol. 31:94-100. https://doi.org/10.1097/MOL.0000000000000665
Shokrzadeh, M., N. Ahangar, M. Zargari, Z. Gilani, A. Shadboorestan, & M. Omidi. 2013. Protective effect of L-carnitine on level of malondialdehyde in diazinon-induced lipid peroxidation in rats. Jou. Maz. Uni. Med. Sci. 22:198-206.
Sun, S., F. Xie, Q. Zhang, Z. Cui, X. Cheng, F. Zhong, K. He, & J. Zhou. 2017. Advanced oxidation protein products induce hepatocyte epithelial–mesenchymal transition via a ROS‐dependent, TGF‐β/Smad signaling pathway. Cell. Biol. Int. 41:842-853. https://doi.org/10.1002/cbin.10792
Sun, W. H., F. Liu, Y. Chen, & Y. C. Zhu. 2012. Hydrogen sulfide decreases the levels of ROS by inhibiting mitochondrial complex IV and increasing SOD activities in cardiomyocytes under ischemia/reperfusion. Biochem. Biophys. Res. Commun. 421:164-169. https://doi.org/10.1016/j.bbrc.2012.03.121
Sung, C. C., Y. C. Hsu, C. C. Chen, Y. F. Lin, & C. C. Wu. 2013. Oxidative stress and nucleic acid oxidation in patients with chronic kidney disease. Oxid. Med. Cell. Longev. 2013:301982. https://doi.org/10.1155/2013/301982
Surai, P. F. 2015. Antioxidant action of carnitine: Molecular mechanisms and practical applications. EC. Vet. Sci. 2:66-84.
Torquato, P., R. Marinelli, D. Bartolini, & F. Galli. 2020. Vitamin E: Nutritional aspects. Mol. Nut. 2020:447-485. Mol. Nutr. https://doi.org/10.1016/B978-0-12-811907-5.00019-1
Vitti, M., G. D. Emidio, M. D. Carlo, G. Carta, A. Antonosante, P. G. Artini, A. Cimini, C. Tatone, & E. Benedetti. 2016. Peroxisome proliferator-activated receptors in female reproduction and fertility. PPAR. Res. 2016:4612306. https://doi.org/10.1155/2016/4612306
Wang, Q. L., J. L. Yuan, Y. Y. Tao, Y. Zhang, P. Liu, & C. H. Liu. 2010. Fuzheng Huayu recipe and vitamin E reverse renal interstitial fibrosis through counteracting TGF-β1-induced epithelial-to-mesenchymal transition. J. Ethnopharmacol. 127:631-640. https://doi.org/10.1016/j.jep.2009.12.011
Wiemer, E. A. 2011. Stressed tumor cell, chemosensitized cancer. Nat. Med. 17:1552-1554. https://doi.org/10.1038/nm.2593
Yang, J., Y. Zhang, X. Xu, J. Li, F. Yuan, S. Bo, J. Qiao, G. Xia, Y. Su, & M. Zhang. 2019. Transforming growth factor-β is involved in maintaining oocyte meiotic arrest by promoting natriuretic peptide type C expression in mouse granulosa cells. Cell Death Dis. 10:558. https://doi.org/10.1038/s41419-019-1797-5
Zarezadeh, R., A. Mehdizadeh, J. L. Leroy, M. Nouri, S. Fayezi, & M. Darabi. 2019. Action mechanisms of n‐3 polyunsaturated fatty acids on the oocyte maturation and developmental competence: Potential advantages and disadvantages. J. Cell. Physiol. 234:1016-1029. https://doi.org/10.1002/jcp.27101
Zhang, X., R. K. Sharma, A. Agarwal, & T. Falcone. 2005. Effect of pentoxifylline in reducing oxidative stress-induced embryotoxicity. J. Assist. Reprod. Genet. 22:415-417.
https://doi.org/10.1007/s10815-005-7202-6
Zhou, S., Y. Ma, J. Yao, A. Zhao, C. Xie, Y. Mi, & C. Zhang. 2021. TGF‐β1‐induced collagen promotes chicken ovarian follicle development via an intercellular cooperative pattern. Cell. Biol. Int. 45:1336-1348. https://doi.org/10.1002/cbin.11580
Authors
HatamiM., YarahmadiH. M., FakhraeiJ., & AhmadiA. (2022). Numbers of Follicles, Pregnancy, Expression of Reactive Oxygen Species (ROS), and Ovarian Genes in Sheep Treated with Vitamin E, L-Carnitine, and Fish Oil. Tropical Animal Science Journal, 45(4), 413-422. https://doi.org/10.5398/tasj.2022.45.4.413
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