Abstract
Selenium (Se) is an essential trace element with important functions in animals and whose deficiency is associated with reproductive failures. The aim of this study was to investigate the effect of Se concentrations during in vitro maturation (IVM) of Bos taurus oocyte within the reference ranges for Se status in cattle. For this purpose, Aberdeen Angus cumulus–oocyte complexes (COCs) were matured in IVM medium supplemented with 0, 10, 50, and 100 ng/mL Se (control, deficient, marginal, and adequate, respectively). The results demonstrated that marginal and adequate Se concentrations added during IVM increased viability and non-apoptotic cumulus cells (CC). Moreover, the addition of Se to culture media decreased malondialdehyde level in COC with all studied concentrations and increased total glutathione content in CC and oocytes with 10 ng/mL Se. On the other hand, total antioxidant capacity of COC, nuclear maturation, and the developmental capacity of oocytes were not modified by Se supplementation. However, 10 ng/mL Se increased hatching rate. In conclusion, supplementation with 10 ng/mL Se during in vitro maturation of Bos primigenius taurus oocytes should be considered to improve embryo quality.
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References
Boland MP (2003) Trace minerals in production and reproduction in dairy cows Adv dairy technol 15:319
Mehdi Y, Dufrasne I (2016) Selenium in cattle: a review. Molecules 21:545. https://doi.org/10.3390/molecules21040545
Singh AK, Rajak SK, Kumar P, Shilpi Kerketta Yogi RK (2018) Nutrition and bull fertility: a review. J Entomol Zool Stud 6(6):635–643
Ahsan U, Kamran Z, Raza I, Ahmad S, Babar W, Riaz MH, Iqbal Z (2014) Role of selenium in male reproduction - a review. Anim Reprod Sci 146:55–62
Wu ASH, Oldfield JE, Shull LR, Cheeke PR (1979) Specific effect of selenium deficiency on rat sperm. Biol Reprod 20:793–798. https://doi.org/10.1095/biolreprod20.4.793
Behne D, Weiler H, Kyriakopoulos A (1996) Effects of selenium deficiency on testicular morphology and function in rats. Reproduction 106:291–297. https://doi.org/10.1530/jrf.0.1060291
Kaur R, Kaur K (2000) Effects of dietary selenium (SE) on morphology of testis and cauda epididymis in rats. Indian J Physiol Pharmacol 44:265–272
Marai IFM, El-Darawany A-HA, Ismail E-SA-F, Abdel-Hafez MAM (2009) Reproductive and physiological traits of Egyptian Suffolk rams as affected by selenium dietary supplementation and housing heat radiation effects during winter of the sub-tropical environment of Egypt (Short Communication). Arch Anim Breed 52:402–409. https://doi.org/10.5194/aab-52-402-2009
Spears JW, Weiss WP (2008) Role of antioxidants and trace elements in health and immunity of transition dairy cows. Vet J 176:70–76. https://doi.org/10.1016/j.tvjl.2007.12.015
Hefnawy AEG, Tórtora-Pérez JL (2010) The importance of selenium and the effects of its deficiency in animal health. Small Ruminant Res 89:185–192. https://doi.org/10.1016/j.smallrumres.2009.12.042
Sordillo LM (2013) Selenium-dependent regulation of oxidative stress and immunity in periparturient dairy cattle. Vet Med Int 2013:154045. https://doi.org/10.1155/2013/154045
Kommisrud E, Osterås O, Vatn T (2005) Blood selenium associated with health and fertility in Norwegian dairy herds. Acta Vet Scand 46:229–240
Schrauzer GN (2000) Selenomethionine: a review of its nutritional significance, metabolism and toxicity. J Nutr 130:1653–1656. https://doi.org/10.1093/jn/130.7.1653
Pehrson B, Hakkarainen J, Työppönen J (1986) Nutritional muscular degeneration in young heifers. Nord Vet Med 38:26–30
Smith KL, Hogan JS, Conrad HR (1988) Selenium in dairy cattle: Its role in disease resistance. Vet Med 83:72–78
Gerloff BJ (1992) Effect of selenium supplementation on dairy cattle. J Anim Sci 70:3934–3940
Ceballos MA, Wittwer F (1996) Metabolismo del selenio en rumiantes. Arch Med Vet XXVIII:15
Brigelius-Flohé R, Maiorino M (2013) Glutathione peroxidases. Biochim Biophys Acta 1830:3289–3303. https://doi.org/10.1016/j.bbagen.2012.11.020
Rivera RE, Christensen VL, Edens FW, Wineland MJ (2005) Influence of selenium on heat shock protein 70 expression in heat stressed turkey embryos (Meleagris gallopavo). Comp Biochem Physiol Part A Mol Integr Physiol 142:427–432. https://doi.org/10.1016/j.cbpa.2005.09.006
Zeng H (2009) Selenium as an essential micronutrient: roles in cell cycle and apoptosis. Molecules 14:1263–1278. https://doi.org/10.3390/molecules14031263
Gopalakrishna R, Chen ZH, Gundimeda U (1997) Selenocompounds induce a redox modulation of protein kinase C in the cell, compartmentally independent from cytosolic glutathione: its role in inhibition of tumor promotion. Arch Biochem Biophys 348:37–48. https://doi.org/10.1006/abbi.1997.0335
Fontenelle LC, Feitosa MM, Morais JBS et al (2018) The role of selenium in insulin resistance. Braz J Pharm Sci 54:1–11. https://doi.org/10.1590/s2175-97902018000100139
Raghu HM, Reddy SM, Nandi S (2002) Effect of insulin, transferrin and selenium and epidermal growth factor on development of buffalo oocytes to the blastocyst stage in vitro in serum-free, semidefined media. Vet Rec 151:260–265. https://doi.org/10.1136/vr.151.9.260
Jeong YW, Hossein MS, Bhandari DP, Kim YW, Kim JH, Park SW, Lee E, Park SM, Jeong YI, Lee JY, Kim S, Hwang WS (2008) Effects of insulin-transferrin-selenium in defined and porcine follicular fluid supplemented IVM media on porcine IVF and SCNT embryo production. Anim Reprod Sci 106:13–24. https://doi.org/10.1016/j.anireprosci.2007.03.021
Córdova B, Morató R, Izquierdo D, Paramio T, Mogas T (2010) Effect of the addition of insulin-transferrin-selenium and/or L-ascorbic acid to the in vitro maturation of prepubertal bovine oocytes on cytoplasmic maturation and embryo development. Theriogenology 74:1341–1348. https://doi.org/10.1016/j.theriogenology.2010.06.003
Makki M, Saboori E, Sabbaghi MA et al (2012) Effects of selenium, calcium and calcium ionophore on human oocytes in vitro maturation in a chemically defined medium. Iran J Reprod Med 10:343–348
Baker RD, Baker SS, Rao R (1998) Selenium deficiency in tissue culture: implications for oxidative metabolism. J Pediatr Gastroenterol Nutr 27:387–392
Xiong X, Lan D, Li J, Lin Y, Li M (2018) Selenium supplementation during in vitro maturation enhances meiosis and developmental capacity of yak oocytes. Anim Sci J 89:298–306. https://doi.org/10.1111/asj.12894
Anchordoquy JP, Anchordoquy JM, Sirini MA, Mattioli G, Picco SJ, Furnus CC (2013) Effect of different manganese concentrations during in vitro maturation of bovine oocytes on DNA integrity of cumulus cells and subsequent embryo development. Reprod Domest Anim 48:905–911. https://doi.org/10.1111/rda.12184
Picco SJ, Anchordoquy JM, de Matos DG et al (2010) Effect of increasing zinc sulphate concentration during in vitro maturation of bovine oocytes. Theriogenology 74:1141–1148. https://doi.org/10.1016/j.theriogenology.2010.05.015
Picco SJ, Rosa DE, Anchordoquy JP, Anchordoquy JM, Seoane A, Mattioli GA, Furnus CC (2012) Effects of copper sulphate concentrations during in vitro maturation of bovine oocytes. Theriogenology 77:373–381. https://doi.org/10.1016/j.theriogenology.2011.08.009
Parrish JJ, Susko-Parrish JL, Leibfried-Rutledge ML, Critser ES, Eyestone WH, First NL (1986) Bovine in vitro fertilization with frozen-thawed semen. Theriogenology 25:591–600
Tervit HR, Whittingham DG, Rowson LE (1972) Successful culture in vitro of sheep and cattle ova. J Reprod Fertil 30:493–49734
Gardner DK, Lane M, Spitzer A, Batt PA (1994) Enhanced rates of cleavage and development for sheep zygotes cultured to the blastocyst stage in vitro in the absence of serum and somatic cells: amino acids, vitamins, and culturing embryos in groups stimulate development. Biol Reprod 50:390–400
Anchordoquy JP, Anchordoquy JM, Pascua AM et al (2017) The copper transporter (SLC31A1/CTR1) is expressed in bovine spermatozoa and oocytes: Copper in IVF medium improves sperm quality. Theriogenology 97:124–133. https://doi.org/10.1016/j.theriogenology.2017.04.037
Izadyar F, Colenbrander B, Bevers MM (1997) Stimulatory effect of growth hormone on in vitro maturation of bovine oocytes is exerted through the cyclic adenosine 3’,5’-monophosphate signaling pathway. Biol Reprod 57:1484–1489
Süss U, Wüthrich K, Stranzinger G (1988) Chromosome configurations and time sequence of the first meiotic division in bovine oocytes matured in vitro. Biol Reprod 38:871–880
Glander HJ, Schaller J (1999) Binding of annexin V to plasma membranes of human spermatozoa: a rapid assay for detection of membrane changes after cryostorage. Mol Hum Reprod 5:109–115
Paasch U, Sharma RK, Gupta AK et al (2004) Cryopreservation and thawing is associated with varying extent of activation of apoptotic machinery in subsets of ejaculated human spermatozoa. Biol Reprod 71:1828–1837. https://doi.org/10.1095/biolreprod.103.025627
Furnus CC, de Matos DG, Moses DF (1998) Cumulus expansion during in vitro maturation of bovine oocytes: relationship with intracellular glutathione level and its role on subsequent embryo development. Mol Reprod Dev 51:76–83. https://doi.org/10.1002/(SICI)1098-2795(199809)51:1<76::AID-MRD9>3.0.CO;2-T
Mauro MO, Sartori D, Oliveira RJ, Ishii PL, Mantovani MS, Ribeiro LR (2011) Activity of selenium on cell proliferation, cytotoxicity, and apoptosis and on the expression of CASP9, BCL-XL and APC in intestinal adenocarcinoma cells. Mutat Res 715:7–12. https://doi.org/10.1016/j.mrfmmm.2011.06.015
Zou Y, Shao J, Li Y, et al (2019) Protective effects of inorganic and organic selenium on heat stress in bovine mammary epithelial cells. In: Oxidative medicine and cellular longevity. https://www.hindawi.com/journals/omcl/2019/1503478/. Accessed 28 Mar 2019
Uhm SJ, Gupta MK, Yang JH, Lee SH, Lee HT (2007) Selenium improves the developmental ability and reduces the apoptosis in porcine parthenotes. Mol Reprod Dev 74:1386–1394. https://doi.org/10.1002/mrd.20701
Sunde RA (1990) Molecular biology of selenoproteins. Annu Rev Nutr 10:451–474. https://doi.org/10.1146/annurev.nu.10.070190.002315
Mihailović M, Cvetković M, Ljubić A, Kosanović M, Nedeljković S, Jovanović I, Pesut O (2000) Selenium and malondialdehyde content and glutathione peroxidase activity in maternal and umbilical cord blood and amniotic fluid. Biol Trace Elem Res 73:47–54. https://doi.org/10.1385/BTER:73:1:47
Ansar S, Alshehri SM, Abudawood M, Hamed SS, Ahamad T (2017) Antioxidant and hepatoprotective role of selenium against silver nanoparticles. Int J Nanomedicine 12:7789–7797. https://doi.org/10.2147/IJN.S136748
Ceko MJ, Hummitzsch K, Hatzirodos N, Bonner WM, Aitken JB, Russell DL, Lane M, Rodgers RJ, Harris HH (2015) X-Ray fluorescence imaging and other analyses identify selenium and GPX1 as important in female reproductive function. Metallomics 7:71–82. https://doi.org/10.1039/c4mt00228h
Abedelahi A, Salehnia M, Allameh AA, Davoodi D (2010) Sodium selenite improves the in vitro follicular development by reducing the reactive oxygen species level and increasing the total antioxidant capacity and glutathione peroxide activity. Hum Reprod 25:977–985. https://doi.org/10.1093/humrep/deq002
Basini G, Tamanini C (2000) Selenium stimulates estradiol production in bovine granulosa cells: possible involvement of nitric oxide. Domest Anim Endocrinol 18:1–17. https://doi.org/10.1016/S0739-7240(99)00059-4
Paszkowski T, Traub AI, Robinson SY, McMaster D (1995) Selenium dependent glutathione peroxidase activity in human follicular fluid. Clin Chim Acta 236:173–180
Shamsuddin M, Larsson B, Gustafsson H, Rodriguez-Martinez H (1994) A serum-free, cell-free culture system for development of bovine one-cell embryos up to blastocyst stage with improved viability. Theriogenology 41:1033–1043
de Matos DG, Furnus CC, Moses DF, Baldassarre H (1995) Effect of cysteamine on glutathione level and developmental capacity of bovine oocyte matured in vitro. Mol Reprod Dev 42:432–436. https://doi.org/10.1002/mrd.1080420409
Funahashi H, Day BN (1995) Effect of cumulus cells on glutathione content of porcine oocytes during in vitro maturation. J Anim Sci 73(1):90
Miyamura M, Yoshida M, Hamano S, Kuwayama M (1995) Glutathione concentration during maturation and fertilization in bovine oocytes. Theriogenology 43(1):282
de Matos DG, Furnus CC, Moses DF, Martinez AG, Matkovic M (1996) Stimulation of glutathione synthesis of in vitro matured bovine oocytes and its effect on embryo development and freezability. Mol Reprod Dev 45:451–457. https://doi.org/10.1002/(SICI)1098-2795(199612)45:4<451::AID-MRD7>3.0.CO;2-Q
Batist G, Katki AG, Klecker RW, Myers CE (1986) Selenium-induced cytotoxicity of human leukemia cells: interaction with reduced glutathione. Cancer Res 46:5482–5485
Stadtman TC (1996) Selenocysteine. Annu Rev Biochem 65:83–100
Lee KH, Jeong D (2012) Bimodal actions of selenium essential for antioxidant and toxic pro-oxidant activities: the selenium paradox (Review). Mol Med Rep 5:299–304. https://doi.org/10.3892/mmr.2011.651
Shalini S, Bansal MP (2007) Co-operative effect of glutathione depletion and selenium induced oxidative stress on API and NFkB expression in testicular cells in vitro: insights to regulation of spermatogenesis. Biol Res 40:307–317 https://doi.org//S0716-97602007000400005
Funding
We are grateful to Centro de Inseminación Artificial La Elisa S.A. (CIALE) for providing bovine frozen semen, and the Staff of SENASA from Frigorífico Gorina S.A. for providing the bovine ovaries. This work was supported by Grant PICT 2015-2154 from Agencia Nacional de Promoción Científica y Tecnológica de la República Argentina (MINCyT). Thanks are also due to A. Di Maggio for manuscript correction and edition.
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R.M.L. and J.M.A. designed the study, E.M.G., N.A.F., and A.C-M. assisted with data collection. C.C.F. and G.A.M analyzed the data and J.P.A. coordinated the experiments and revised the manuscript. All co-authors participated in lab work.
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Lizarraga, R.M., Anchordoquy, J.M., Galarza, E.M. et al. Sodium Selenite Improves In Vitro Maturation of Bos primigenius taurus Oocytes. Biol Trace Elem Res 197, 149–158 (2020). https://doi.org/10.1007/s12011-019-01966-2
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DOI: https://doi.org/10.1007/s12011-019-01966-2