journal article Jul 03, 2018

a-Tocopherol modifies the expression of genes related to oxidative stress and apoptosis during in vitro maturation and enhances the developmental competence of rabbit oocytes

Abstract
The developmental competence of in vitro maturation (IVM) oocytes can be enhanced by antioxidant agents. The present study investigated, for the first time in the rabbit model, the effect of adding a-tocopherol (0, 100, 200 and 400 µM) during IVM on putative transcripts involved in antioxidant defence (superoxide dismutase 2, mitochondrial (SOD2), glutathione peroxidase 1 (GPX1), catalase (CAT)), cell cycle regulation and apoptosis cascade (apoptosis tumour protein 53 (TP53), caspase 3, apoptosis-related cysteine protease (CASP3)), cell cycle progression (cellular cycle V-Akt murine thymoma viral oncogene homologue 1 (AKT1)), cumulus expansion (gap junction protein, alpha 1, 43 kDa (GJA1) and prostaglandin-endoperoxide synthase 2 (prostaglandin G/H synthase and cyclo-oxygenase) (PTGS2)) and metabolism (glucose-6-phosphate dehydrogenase (G6PD)). Meiotic progression, mitochondrial reallocation, cumulus cell apoptosis and the developmental competence of oocytes after IVF were also assessed. Expression of SOD2, CAT, TP53, CASP3 and GJA1 was downregulated in cumulus–oocyte complexes (COCs) after IVM with 100 µM a-tocopherol compared with the group without the antioxidant. The apoptotic rate and the percentage of a non-migrated mitochondrial pattern were lower in COCs cultured with 100 µM a-tocopherol, consistent with better-quality oocytes. In fact, early embryo development was improved when 100 µM a-tocopherol was included in the IVM medium, but remained low compared with in vivo-matured oocytes. In conclusion, the addition of 100 µM a-tocopherol to the maturation medium is a suitable approach to manage oxidative stress and apoptosis, as well as for increasing the invitro developmental competence of rabbit oocytes.
Topics

No keywords indexed for this article. Browse by subject →

References
62
[1]
Adeldust "In vitro maturation of ovine oocyte in a modified granulosa cells co-culture system and alpha-tocopherol supplementation effects on nuclear maturation and cleavage." J. Anim. Sci. Technol. (2015) 10.1186/s40781-015-0061-5
[2]
Agarwal "The effects of oxidative stress on female reproduction a review." Reprod. Biol. Endocrinol. (2012) 10.1186/1477-7827-10-49
[3]
Arias-Álvarez "Influence of hormonal and nonhormonal estrus synchronization methods on follicular and oocyte quality in primiparous lactating does at early postpartum period." Theriogenology (2010) 10.1016/j.theriogenology.2009.07.017
[4]
Arias-Álvarez "Ovarian response and embryo gene expression patterns after nonsuperovulatory gonadotropin stimulation in primiparous rabbits does." Theriogenology (2013) 10.1016/j.theriogenology.2012.09.019
[5]
In vivo and in vitro maturation of rabbit oocytes differently affects the gene expression profile, mitochondrial distribution, apoptosis and early embryo development

M. Arias-Álvarez, R. M. García-García, J. López-Tello et al.

Reproduction, Fertility and Development 2017 10.1071/rd15553
[6]
Asadi "Effect of vitamin E on oocytes apoptosis in nicotine-treated mice." Iran. J. Basic Med. Sci. (2012)
[7]
Assidi "Identification of potential markers of oocyte competence expressed in bovine cumulus cells matured with follicle-stimulating hormone and/or phorbol myristate acetate in vitro." Biol. Reprod. (2008) 10.1095/biolreprod.108.067686
[8]
Azzi "Vitamin E: non-antioxidant roles." Prog. Lipid Res. (2000) 10.1016/s0163-7827(00)00006-0
[9]
Bermejo-Alvarez "Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts." Proc. Natl. Acad. Sci. USA (2010) 10.1073/pnas.0913843107
[10]
Cassano "Antioxidant defense in the follicular fluid of water buffalo." Cell. Physiol. Biochem. (1999) 10.1159/000016307
[11]
Chow "Vitamin E and oxidative stress." Free Radic. Biol. Med. (1991) 10.1016/0891-5849(91)90174-2
[12]
Combelles "Could oxidative stress influence the in-vitro maturation of oocytes?" Reprod. Biomed. Online (2009) 10.1016/s1472-6483(10)60038-7
[13]
Dalvit "Effect of alpha-tocopherol and ascorbic acid on bovine oocyte in vitro maturation." Reprod. Domest. Anim. (2005) 10.1111/j.1439-0531.2004.00522.x
[14]
Davis "Anovulation in cyclooxygenase-2-deficient mice is restored by prostaglandin E2 and interleukin-1beta." Endocrinology (1999) 10.1210/endo.140.6.6715
[15]
Duggavathi "Ovulation signals." Science (2009) 10.1126/science.1174130
[16]
Edry "Meiotic arrest of oocytes depends on cell-to-cell communication in the ovarian follicle." Mol. Cell. Endocrinol. (2006) 10.1016/j.mce.2006.03.009
[17]
El Mouatassim "Expression of genes encoding antioxidant enzymes in human and mouse oocytes during the final stages of maturation." Mol. Hum. Reprod. (1999) 10.1093/molehr/5.8.720
[18]
Transgenic rabbits as therapeutic protein bioreactors and human disease models

Jianglin Fan, Teruo Watanabe

Pharmacology & Therapeutics 2003 10.1016/s0163-7258(03)00069-x
[19]
Fan "MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility." Science (2009) 10.1126/science.1171396
[20]
Farzollahi "Supplementation of culture media with vitamin E improves mouse antral follicle maturation and embryo development from vitrified ovarian tissue." J. Obstet. Gynaecol. Res. (2016) 10.1111/jog.12933
[21]
Feuerstein "Gene expression in human cumulus cells one approach to oocyte competence." Hum. Reprod. (2007) 10.1093/humrep/dem336
[22]
Rabbit as a reproductive model for human health

Bernd Fischer, Pascale Chavatte-Palmer, Christoph Viebahn et al.

Reproduction 2012 10.1530/rep-12-0091
[23]
Gall "Protein phosphorylation pattern during in vitro maturation of goat oocytes." Mol. Reprod. Dev. (1993) 10.1002/mrd.1080360415
[24]
Garcia-Garcia "ß-Nerve growth factor identification in male rabbit genital tract and seminal plasma and its role in ovulation induction in rabbit does." Ital. J. Anim. Sci. (2018) 10.1080/1828051x.2017.1382315
[25]
Gittens "Differential contributions of connexin37 and connexin43 to oogenesis revealed in chimeric reaggregated mouse ovaries." J. Cell Sci. (2005) 10.1242/jcs.02624
[26]
Guérin "Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings." Hum. Reprod. Update (2001) 10.1093/humupd/7.2.175
[27]
Hoshino "Protein kinase B (PKB/Akt) is required for the completion of meiosis in mouse oocytes." Dev. Biol. (2008) 10.1016/j.ydbio.2007.12.005
[28]
Jang "Cumulus cell-expressed type I interferons induce cumulus expansion in mice." Biol. Reprod. (2015) 10.1095/biolreprod.114.122770
[29]
Jeong "Antiapoptotic and embryotrophic effects of alpha-tocopherol and l-ascorbic acid on porcine embryos derived from in vitro fertilization and somatic cell nuclear transfer." Theriogenology (2006) 10.1016/j.theriogenology.2006.06.007
[30]
Kastrop "Changes in protein synthesis and phosphorylation patterns during bovine oocyte maturation in vitro." J. Reprod. Fertil. (1990) 10.1530/jrf.0.0900305
[31]
Khalil "Protective effects of antioxidants on linoleic acid-treated bovine oocytes during maturation and subsequent embryo development." Theriogenology (2013) 10.1016/j.theriogenology.2013.04.008
[32]
Khan "Diffused intra-oocyte hydrogen peroxide activates myeloperoxidase and deteriorates oocyte quality." PLoS One (2015) 10.1371/journal.pone.0132388
[33]
[34]
Kowaltowski "Mitochondria and reactive oxygen species." Free Radic. Biol. Med. (2009) 10.1016/j.freeradbiomed.2009.05.004
[35]
López-Tello "The effects of sildenafil citrate on feto-placental development and haemodynamics in a rabbit model of intrauterine growth restriction." Reprod. Fertil. Dev. (2017) 10.1071/rd15330
[36]
Lord "Oxidative stress and ageing of the post-ovulatory oocyte." Reproduction (2013) 10.1530/rep-13-0111
[37]
Lorenzo "Stimulatory effect of insulin-like growth factor I and epidermal growth factor on the maturation of rabbit oocytes in vitro." J. Reprod. Fertil. (1996) 10.1530/jrf.0.1070109
[38]
Marques "Melatonin reduces apoptotic cells, SOD2 and HSPB1 and improves the in vitro production and quality of bovine blastocysts." Reprod. Domest. Anim. (2018) 10.1111/rda.13097
[39]
Martín-Romero "Contribution of culture media to oxidative stress and its effect on human oocytes." Reprod. Biomed. Online (2008) 10.1016/s1472-6483(10)60312-4
[40]
McCluskey "Alpha-tocopherol inhibits oxidative stress induced by cholestanetriol and 25-hydroxycholesterol in porcine ovarian granulosa cells." Mol. Cell. Biochem. (1999) 10.1023/a:1006967219894
[41]
McKenzie "Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF." Hum. Reprod. (2004) 10.1093/humrep/deh535
[42]
Motlik "Interplay between CDC2 kinase and MAP kinase pathway during maturation of mammalian oocytes." Theriogenology (1998) 10.1016/s0093-691x(97)00418-4
[43]
Natarajan "Effect of a-tocopherol supplementation on in vitro maturation of sheep oocytes and in vitro development of preimplantation sheep embryos to the blastocyst stage." J. Assist. Reprod. Genet. (2010) 10.1007/s10815-010-9430-7
[44]
Differential development of rabbit embryos following microinsemination with sperm and spermatids

Narumi Ogonuki, Kimiko Inoue, Hiromi Miki et al.

Molecular Reproduction and Development 2005 10.1002/mrd.20363
[45]
Olson "Culture of in vitro-produced bovine embryos with vitamin E improves development in vitro and after transfer to recipients." Biol. Reprod. (2000) 10.1095/biolreprod62.2.248
[46]
Palini "Influence of ovarian stimulation for IVF/ICSI on the antioxidant defence system and relationship to outcome." Reprod. Biomed. Online (2014) 10.1016/j.rbmo.2014.03.010
[47]
Rizos "Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo implications for blastocyst yield and blastocyst quality." Mol. Reprod. Dev. (2002) 10.1002/mrd.1153
[48]
Savitskaya "Mechanisms of apoptosis." Biochemistry (2015) 10.1134/s0006297915110012
[49]
Analyzing real-time PCR data by the comparative CT method

Thomas D Schmittgen, Kenneth J Livak

Nature Protocols 2008 10.1038/nprot.2008.73
[50]
Schweigert "Concentrations of carotenoids, retinol and a-tocopherol in plasma and follicular fluid of women undergoing IVF." Hum. Reprod. (2003) 10.1093/humrep/deg249

Showing 50 of 62 references

Metrics
24
Citations
62
References
Details
Published
Jul 03, 2018
Vol/Issue
30(12)
Pages
1728-1738
License
View
Cite This Article
M. Arias-Álvarez, R. M. García-García, J. López-Tello, et al. (2018). a-Tocopherol modifies the expression of genes related to oxidative stress and apoptosis during in vitro maturation and enhances the developmental competence of rabbit oocytes. Reproduction, Fertility and Development, 30(12), 1728-1738. https://doi.org/10.1071/rd17525