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l-Ergothioneine improves the developmental potential of in vitro sheep embryos without influencing OCTN1-mediated cross-membrane transcript expression

Published online by Cambridge University Press:  02 April 2018

A. Mishra*
Affiliation:
ICAR-NIANP, Bangalore 560030, India.
I.J. Reddy
Affiliation:
Animal Biotechnology Laboratory, ICAR-National Institute of Animal Nutrition and Physiology, Adugodi, Bangalore 560 030, India.
A. Dhali
Affiliation:
OMICS Laboratory, ICAR-National Institute of Animal Nutrition and Physiology Adugodi, Bangalore 560 030, India.
P.K. Javvaji
Affiliation:
OMICS Laboratory, ICAR-National Institute of Animal Nutrition and Physiology Adugodi, Bangalore 560 030, India.
*
All correspondence to: Ashish Mishra. ICAR-NIANP, Bangalore 560030, India. Tel: +91 80 25711304. E-mail: ashishvet1@gmail.com

Summary

The objective of the study was to investigate the effect of l-ergothioneine (l-erg) (5 mM or 10 mM) supplementation in maturation medium on the developmental potential and OCTN1-dependant l-erg-mediated (10 mM) change in mRNA abundance of apoptotic (Bcl2, Bax, Casp3 and PCNA) and antioxidant (GPx, SOD1, SOD2 and CAT) genes in sheep oocytes and developmental stages of embryos produced in vitro. Oocytes matured with l-erg (10 mM) reduced their embryo toxicity by decreasing intracellular ROS and increasing intracellular GSH in matured oocytes that in turn improved developmental potential, resulting in significantly (P < 0.05) higher percentages of cleavage (53.72% vs 38.86, 46.56%), morulae (34.36% vs 20.62, 25.84%) and blastocysts (14.83% vs 6.98, 9.26%) compared with other lower concentrations (0 mM and 5 mM) of l-erg without change in maturation rate. l-Erg (10 mM) treatment did not influence the mRNA abundance of the majority of apoptotic and antioxidant genes studied in the matured oocytes and developmental stages of embryo. A gene expression study found that the SLC22A4 gene that encodes OCTN1, an integral membrane protein and specific transporter of l-erg was not expressed in oocytes and developmental stages of embryos. Therefore it was concluded from the study that although there was improvement in the developmental potential of sheep embryos by l-erg supplementation in maturation medium, there was no change in the expression of the majority of the genes studied due to the absence of the SLC22A4 gene in oocytes and embryos that encode OCTN1, which is responsible for transportation of l-erg across the membrane to alter gene expression.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

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References

Abdelrazik, H., Sharma, R., Mahfouz, R. & Agarwal, A. (2009). l-Carnitine decreases DNA damage and improves the in vitro blastocyst development rate in mouse embryos. Fertil. Steril. 91, 589–96.CrossRefGoogle ScholarPubMed
Agarwal, A., Gupta, S., & Sharma, R. K. (2005). Role of oxidative stress in female reproduction. Reprod. Biol. And Endocrinol. 3, 28.CrossRefGoogle ScholarPubMed
Agarwal, A., Aponte-Mellado, A., Premkumar, B.J., Shaman, A. &; Gupta, S. (2012). The effects of oxidative stress on female reproduction: a review. Reprod. Biol. Endocrinol. 10, 4980.CrossRefGoogle ScholarPubMed
Akanmu, D., Cecchini, R., Aruoma, O.I. & Halli, B. (1991). The antioxidant action of ergothioneine. Arch. Biochem. Biophys. 288, 10–6.CrossRefGoogle ScholarPubMed
Aruoma, O.I., Sunb, B., Fujii, H., Neergheen, V.S., Bahorun, T., Kang, K.S. & Sung, M.K. (2006). Low molecular proanthocyanidin dietary biofactor Oligonol: Its modulation of oxidative stress, bioefficacy, neuroprotection, food application and chemoprevention potentials. BioFactors 27, 245–65.CrossRefGoogle ScholarPubMed
Cheah, I.K. & Halliwell, B. (2012). Ergothioneine; antioxidant potential, physiological function and role in disease. Biochim. Biophys. Acta 1822, 784–93.CrossRefGoogle ScholarPubMed
Correa, G.A., Rumpf, R., Mundim, T.C.D., Franco, M.M. & Dode, M.A.N. (2008). Oxygen tension during in vitro culture of bovine embryos: effect in production and expression of genes related to oxidative stress. Anim. Reprod. Sci. 104, 132–42.CrossRefGoogle ScholarPubMed
Elamaran, G., Singh, K.P., Singh, M.K., Singla, S.K., Chauhan, M.S., Manik, R.S. & Palta, P. (2012). Oxygen concentration and cysteamine supplementation during in vitro production of buffalo Bubalus bubalis embryos affect mRNA expression of BCL-2, BCL-XL, MCL-1, BAX and BID. Reprod. Dom. Anim. 47, 1027–36.CrossRefGoogle ScholarPubMed
Flentjar, N.J., Crack, P.J., Boyd, R., Malin, M., De Haan, J.B., Hertzog, P., Kola, I. & Iannello, R. (2002). Mice lacking glutathione peroxidase-1 activity show increased TUNEL staining and an accelerated inflammatory response in brain following a cold-induced injury. Exp. Neurol. 177, 920.CrossRefGoogle Scholar
Franzoni, R.C., Galeta, F., Laurenza, I., Barsotti, M., Di Stefano, R., Bocchetti, R., Regoli, F., Carpi, A., Balbarini, A., Migliore, L. & Santoro, G. (2006). An in vitro study on the free radical scavenging capacity of ergothionine: comparison with reduced glutathione, uric acid and trolox. Biomed. Pharmacother. 60, 453–7.CrossRefGoogle Scholar
Grigat, S., Harlfinger, S., Pal, S., Striebinger, R., Golz, S., Geerts, A., Lazar, A., Schomig, E. & Grundemann, D. (2007). Probing the substrate specificity of the ergothioneine transporter with methimazole, hercynine, and organic cations. Biochem. Pharmacol. 74, 309–16.CrossRefGoogle ScholarPubMed
Grundemann, D., Harlfinger, S., Goltz, S., Geerts, A., Lazar, A., Berkels, R., Jung, N., Rubbert, A. & Schömig, E. (2005). Discovery of the ergothioneine transporter. Proc. Natl. Acad. Sci. USA 102, 5256–61.CrossRefGoogle ScholarPubMed
Guerin, P., El Mouatassim, S. & Menezo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7, 175–89.CrossRefGoogle ScholarPubMed
Gulcin, I. (2006). Antioxidant antiradical activities of l-carnitine. Life Sci. 78: 803–11.CrossRefGoogle ScholarPubMed
He, T., Peterson, T.E., Holmuhamedov, E.L., Terzic, A., Caplice, N.M., Oberley, L.W. & Katusic, Z.S. (2004). Human endothelial progenitor cells tolerate oxidative stress due to intrinsically high expression of manganese superoxide dismutase. Arterioscler. Thromb. Vasc. Biol. 24, 2021–27.CrossRefGoogle ScholarPubMed
Kang, J.T., Atikuzzaman, M., Kwon, D.K., Park, S.J., Kim, S.J., Moon, J.H., Koo, O.J, Jang, G. & Lee, B.C. (2012). Developmental competence of porcine oocytes after in vitro maturation and in vitro culture under different oxygen concentrations. Zygote 20, 18.CrossRefGoogle ScholarPubMed
Kawano, H., Murata, H., Iriguchi, S., Mayumi, T. & Hama, T. (1983). Studies on ergothioneine XI Inhibitory effect on lipid peroxide formation in mouse liver. Chem. Pharm. Bull. Tokyo 31, 1682–87.CrossRefGoogle ScholarPubMed
Kobayashi, T., Miyazaki, T., Natori, M. & Nozawa, S. (1991). Protective role of superoxide dismutase in human sperm motility: superoxide dismutase activity and lipid peroxide in human seminal plasma and spermatozoa. Hum. Reprod. 67, 987–91.CrossRefGoogle Scholar
Lamhonwah, A.M. & Tein, I. (2006). Novel localization of OCTN1, an organic cation/carnitine transporter, to mammalian mitochondria. Biochem. Biophys. Res. Commun. 345, 1315–25.CrossRefGoogle ScholarPubMed
Lee, B.J., Lin, J.S., Lin, Y.C. & Lin, P.T. (2014). Effect of l-carnitine supplementation on oxidative stress and antioxidant enzymes activities in patients with coronary disease: a randomized, placebo-controlled trial. Nutri. J. 13, 79.CrossRefGoogle ScholarPubMed
Lequarre, A.S., Feugang, J.M., Malhomme, O., Donnay, I., Massip, A., Dessy, F. & Langendonckt, A.V. (2001). Expression of Cu/Zn Mn superoxide dismutase during bovine embryo development: influence of in vitro culture. Mol. Reprod. Dev. 58, 4553.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Mari, M., Morales, A., Colell, A., Garcia-Ruiz, C. and Fernez-Checa, J.C. (2009). Mitochondrial glutathione a key survival antioxidant. Antioxid. Redox. Signal. 11, 26852700.CrossRefGoogle ScholarPubMed
Markova, N.G., Jurukovska, N.K., Dong, K.K., Damaghi, N., Smiles, K.A. and Yarosh, D.B. (2009). Skin cells and tissue are capable of using l-ergothioneine as an integral component of their antioxidant defence system. Free Radic. Biol. Med. 46, 1168–76.CrossRefGoogle Scholar
Mishra, A., Chandra, V. & Sharma, G.T. (2010a). Effect of epidermal growth factor on in vitro maturation of buffalo oocytes and embryo development with insulin like growth factor-1 and β-mercaptoethanol. Ind. J. Anim. Sci. 808, 721–24.Google Scholar
Mishra, A., Sharma, G.T. & Kumar, G.S. (2010b). Expression profile of connexin 43 Cx43 and polyA polymerase PAP genes in buffalo Bubalus bubalis embryos produced in vitro. J. Appl. Anim. Res. 38, 2932.CrossRefGoogle Scholar
Mishra, A., Gupta, P.S.P., Reddy, I.J., Sejian, V. & Ravindra, J.P. (2016a). Maturation timing and fetal bovine serum concentration for developmental potential of sheep oocytes in vitro. Ind. J. Exp. Biol. 54, 630–3.Google ScholarPubMed
Mishra, A., Reddy, I. J, Gupta, P.S.P. & Mondal, S. (2016b). l-Carnitine mediated reduction in oxidative stress and alteration in transcript level of antioxidant enzymes in sheep embryos produced in vitro. Reprod. Dom. Anim. 51, 311–21.CrossRefGoogle ScholarPubMed
Mishra, A., Reddy, I. J, Gupta, P.S.P. & Mondal, S. (2016c). Developmental regulation and modulation of apoptotic genes expression in sheep oocytes and embryos cultured in vitro with l-carnitine. Reprod. Dom. Anim. 51, 1020–9.CrossRefGoogle ScholarPubMed
Mishra, A., Reddy, I. J, Gupta, P.S.P. & Mondal, S. (2017). Expression of apoptotic and antioxidant enzyme genes in sheep oocytes and in vitro produced embryos. Anim. Biotechnol. 281, 1825.CrossRefGoogle Scholar
Motohashi, N., Mori, I., Sugiura, Y. & Tanaka, H. (1974). Metal-complexes of ergothioneine. Chem. Pharm. Bull. 22, 654–7.CrossRefGoogle Scholar
Mukherjee, A., Malik, H., Saha, A.P., Dubey, A., Singhal, D.K., Boateng, S., Saughika, S., Kumar, S., De, S., Guha, S. & Malakar, D. 2014. Resveratrol treatment during oocytes maturation enhances developmental competence of parthenogenetic hand-made cloned blastocysts by modulating intracellular glutathione level embryonic gene expression. J. Assist. Reprod. Gen. 31, 229–39.CrossRefGoogle ScholarPubMed
Nakamura, T., Sugiura, S., Kobayashi, D., Yoshida, K., Yabuuchi, H., Aizawa, S., Maeda, T. & Tamai, I. (2007). Decreased proliferation and erythroid differentiation of K562 cells by siRNA-induced depression of OCTN1 (SLC22A4) transporter gene. Pharm. Res. 24, 1628–35.CrossRefGoogle ScholarPubMed
Obayashi, K., Kurihara, K., Okano, Y., Masaki, H. & Yarosh, D.B. (2005). l-Ergothioneine scavenges superoxide and singlet O and suppresses TNF-α and MMP-1 expression in UV-irradiated human dermal fibroblasts. J. Cosmet. Sci. 56, 1727.Google ScholarPubMed
Ozturkler, Y., Yildiz, S., Gungor, O., Pancarci, S.M., Kaçar, C. & Ari, U.C. (2010). The effects of l-ergothioneine and l-ascorbic acid on the in vitro maturation (IVM) and embryonic development (IVC) of sheep oocytes. Kafkas. Univ. Vet. Fak. Derg. 16, 757–63.Google Scholar
Parrish, J.J., Susko-Parrish, J.L., Winer, M.A. & First, N.L. (1988). Capacitation of bovine sperm by heparin. Biol. Reprod. 38, 1171–80.CrossRefGoogle ScholarPubMed
Sharma, G.T., Majumdar, A.C. & Bonde, S.W. (1996). Chronology of maturational events in goat oocytes cultured in vitro. Small Rumin. Res. 22, 2530.CrossRefGoogle Scholar
Singh, R.P., Shah, R.G. & Tank, P.H. (2012). Influence of different quality of buffalo oocytes on in vitro maturation and fertilization. Ind. J. Anim. Reprod. 33, 913.Google Scholar
Sirard, M.A. and Coenen, K (2006). In vitro maturation and embryo production in cattle. Methods Mol. Biol. 348, 3542.CrossRefGoogle ScholarPubMed
Takahashi, T., Inaba, Y., Somfai, T., Kaneda, M., Geshi, M., Nagai, T. & Manabe, N. 2013. Supplementation of culture medium with l-carnitine improves development cryotolerance of bovine embryos produced in vitro. Reprod. Fert. Dev. 25, 589–99.CrossRefGoogle ScholarPubMed
Urban, T.J., Yang, C., Lagpacan, L.L., Brown, C., Castro, R.A., Taylor, T.R., Huang, C.C., Stryke, D., Johns, S.J, Kawamoto, M., Carlson, E.J., Ferrin, T.E., Burchard, E.G. & Giacomini, K.M. (2007). Functional effects of protein sequence polymorphisms in the organic cation/ergothioneine transporter OCTN1 (SLC22A4). Pharmacogenet. Genomics 17, 773–82.CrossRefGoogle ScholarPubMed
Wrenzycki, C., Hermann, D. & Niemann, H. (2007). Messenger RNA in oocytes and embryos in relation to embryo viability. Theriogenology 68S, S77–83.CrossRefGoogle Scholar
Wu, X., George, R.L., Huang, W., Wang, H., Conway, S.J., Leibach, F.H. & Ganapathy, V. (2000). Structural and functional characteristics and tissue distribution pattern of rat OCTN1, an organic cation transporter, cloned from placenta. Biochim. Biophys. Acta 1466 (1–2), 315–27.CrossRefGoogle ScholarPubMed
You, J., Lee, J., Hyun, S.H. & Eunsong, L. (2012). l-Carnitine treatment during oocyte maturation improves in vitro development of cloned pig embryos by influencing intracellular glutathione synthesis and embryonic gene expression. Theriogenology 78, 235–43.CrossRefGoogle ScholarPubMed
Zhou, W., Xiang, T., Walker, S., Farrar, V., Hwang, E., Findeisen, B., Sadeghieh, S., Arenivas, F., Abruzzese, R.V. & Polejaeva, I. (2008). Global gene expression analysis of bovine blastocysts produced by multiple methods. Mol. Reprod. Dev. 75, 744–58.CrossRefGoogle ScholarPubMed
Zullo, G., Albero, G., Neglia, G., De Canditiis, C., Bifulco, G., Campanile, G. & Gasparrini, B. (2016). l-Ergothioneine supplementation during culture improves quality of bovine in vitro-produced embryos. Theriogenology 85, 688–97.CrossRefGoogle ScholarPubMed