Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-27T15:45:26.478Z Has data issue: false hasContentIssue false
  • English
  • Français

Linolenic acid improves oocyte developmental competence and decreases apoptosis of in vitro-produced blastocysts in goat

Published online by Cambridge University Press:  20 November 2015

Arash Veshkini ,
Ali Akbar Khadem ,
Abdollah Mohammadi-Sangcheshmeh ,
Ali Asadi Alamouti ,
Masoud Soleimani  and
Eduardo L. Gastal
Arash Veshkini
Affiliation:
Department of Animal and Poultry Science, College of Aburaihan, University of Tehran, Pakdasht, Tehran, Iran. Department of Transgenic Animal Science, Stem Cell Technology Research Center, Tehran, Iran.
Ali Akbar Khadem
Affiliation:
Department of Animal and Poultry Science, College of Aburaihan, University of Tehran, Pakdasht, Tehran, Iran.
Abdollah Mohammadi-Sangcheshmeh*
Affiliation:
Department of Animal and Poultry Science, College of Aburaihan, University of Tehran, Pakdasht, Theran P.O.Box: 11365/7117, Iran. Department of Animal and Poultry Science, College of Aburaihan, University of Tehran, Pakdasht, Tehran, Iran.
Ali Asadi Alamouti
Affiliation:
Department of Animal and Poultry Science, College of Aburaihan, University of Tehran, Pakdasht, Tehran, Iran.
Masoud Soleimani
Affiliation:
Department of Hematology, Faculty of Medical Science, Tarbiat Modares University, Tehran, Iran.
Eduardo L. Gastal
Affiliation:
Department of Animal Science, Food and Nutrition, Southern Illinois University, Carbondale, Illinois, USA.
*
All correspondence to: Abdollah Mohammadi-Sangcheshmeh. Department of Animal and Poultry Science, College of Aburaihan, University of Tehran, Pakdasht, Theran P.O.Box: 11365/7117, Iran. Fax: +98 21 36040907. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The effects of α-linolenic acid (ALA) on developmental competence of oocytes in goats were evaluated in this study. Initially, the level of ALA in small and large antral follicles was determined to be in a range of 0.018–0.028 mg/ml (64.6–100.6 μM, respectively). In vitro maturation was performed in the presence of various concentrations (10, 50, 100, or 200 μM) of ALA. Cumulus expansion, meiotic maturation, levels of intracellular glutathione (GSH), embryonic cleavage, blastocyst formation following parthenogenetic activation (PA) and in vitro fertilization (IVF), number of total and apoptotic cells in blastocyst, and expression of Bax, Bcl-2, and p53 genes in blastocyst cells were determined. Compared with the control, no improvement was observed in cumulus expansion in ALA-treated groups. At 50 μM concentration, ALA increased meiotic maturation rate but had no effect on GSH level. When oocytes treated with 50 μM ALA were subsequently used for PA or IVF, a higher rate of blastocyst formation was observed, and these embryos had a higher total cell number and a lower apoptotic cell number. Expression analyses of genes in blastocysts revealed lesser transcript abundances for Bax gene, and higher transcript abundances for Bcl-2 gene in 50 μM ALA group. Expression of p53 gene was also less observed in ALA-treated blastocysts. Our results show that ALA treatment at 50 μM during in vitro maturation (IVM) had a beneficial effect on maturation of goat oocytes and this, in turn, stimulated embryonic development and regulated apoptotic gene expression.

Keywords

Apoptosis genesBlastocystGSH levelGoat oocyteα-Linolenic acid
Type
Research Article
Information
Zygote , Volume 24 , Issue 4 , August 2016 , pp. 537 - 548
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abayasekara, D.R. & Wathes, D.C. (1999). Effects of altering dietary fatty acid composition on prostaglandin synthesis and fertility. Prostag. Leukot. Ess. 61, 275–87.Google Scholar
Abazari-Kia, A.H., Mohammadi-Sangcheshmeh, A., Dehghani-Mohammadabadi, M., Jamshidi-Adegani, F., Veshkini, A., Zhandi, M., Cinar, M.U. & Salehi, M. (2014). Intracellular glutathione content, developmental competence and expression of apoptosis-related genes associated with G6PDH-activity in goat oocyte. J. Assist. Reprod Genet. 31, 313–21.Google Scholar
Al Darwich, A., Perreau, C., Petit, M.H., Papillier, P., Dupont, J., Guillaume, D., Mermillod, P. & Guignot, F. (2010). Effect of PUFA on embryo cryoresistance, gene expression and AMPKalpha phosphorylation in IVF-derived bovine embryos. Prostag. Oth. Lipid M. 93, 30–6.Google Scholar
Amundson, S.A., Myers, T.G. & Fornace, A.J. Jr. (1998). Roles for p53 in growth arrest and apoptosis: putting on the brakes after genotoxic stress. Oncogene 17, 3287–99.Google Scholar
Andrade, L.N., de Lima, T.M., Curi, R. & Castrucci, A.M. (2005). Toxicity of fatty acids on murine and human melanoma cell lines. Toxicol. In Vitro 19, 553–60.CrossRefGoogle ScholarPubMed
Barcelo-Coblijn, G. & Murphy, E.J. (2009). Alpha-linolenic acid and its conversion to longer chain n-3 fatty acids: benefits for human health and a role in maintaining tissue n-3 fatty acid levels. Prog. Lipid Res. 48, 355–74.CrossRefGoogle Scholar
Bender, K., Walsh, S., Evans, A.C., Fair, T. & Brennan, L. (2010). Metabolite concentrations in follicular fluid may explain differences in fertility between heifers and lactating cows. Reproduction 139, 1047–55.Google Scholar
Browne, R.W. & Armstrong, D. (2000). HPLC analysis of lipid-derived polyunsaturated fatty acid peroxidation products in oxidatively modified human plasma. Clin. Chem. 46, 829–36.CrossRefGoogle ScholarPubMed
Burlacu, A. (2003). Regulation of apoptosis by Bcl-2 family proteins. J. Cell. Mol. Med. 7, 249–57.CrossRefGoogle ScholarPubMed
Cha, K.Y. & Chian, R.C. (1998). Maturation in vitro of immature human oocytes for clinical use. Hum. Reprod. Update 4, 103–20.CrossRefGoogle ScholarPubMed
Childs, S., Hennessy, A.A., Sreenan, J.M., Wathes, D.C., Cheng, Z., Stanton, C., Diskin, M.G. & Kenny, D.A. (2008). Effect of level of dietary n-3 polyunsaturated fatty acid supplementation on systemic and tissue fatty acid concentrations and on selected reproductive variables in cattle. Theriogenology 70, 595–611.Google Scholar
Chrenek, P., Kubovicova, E., Olexikova, L., Makarevich, A.V., Toporcerova, S. & Ostro, A. (2014). Effect of body condition and season on yield and quality of in vitro produced bovine embryos. Zygote Epub ahead of print.Google Scholar
Coyral-Castel, S., Rame, C., Fatet, A. & Dupont, J. (2010). Effects of unsaturated fatty acids on progesterone secretion and selected protein kinases in goat granulosa cells. Domest. Anim. Endocrinol. 38, 272–83.CrossRefGoogle ScholarPubMed
Elvin, J.A., Yan, C. & Matzuk, M.M. (2000). Growth differentiation factor-9 stimulates progesterone synthesis in granulosa cells via a prostaglandin E2/EP2 receptor pathway. Proc. Natl. Acad. Sci. USA 97, 10288–93.Google Scholar
Fouladi-Nashta, A.A., Wonnacott, K.E., Gutierrez, C.G., Gong, J.G., Sinclair, K.D., Garnsworthy, P.C. & Webb, R. (2009). Oocyte quality in lactating dairy cows fed on high levels of n-3 and n-6 fatty acids. Reproduction 138, 771–81.CrossRefGoogle ScholarPubMed
Funston, R.N. (2004). Fat supplementation and reproduction in beef females. J. Anim. Sci. 82 (E-Suppl.), E154–61.Google ScholarPubMed
Ghaffarilaleh, V., Fouladi-Nashta, A. & Paramio, M.T. (2014). Effect of alpha-linolenic acid on oocyte maturation and embryo development of prepubertal sheep oocytes. Theriogenology 82, 686–96.Google Scholar
Gladine, C., Rock, E., Morand, C., Bauchart, D. & Durand, D. (2007). Bioavailability and antioxidant capacity of plant extracts rich in polyphenols, given as a single acute dose, in sheep made highly susceptible to lipoperoxidation. Br. J. Nutr. 98, 691–701.Google Scholar
Gross, A., McDonnell, J.M. & Korsmeyer, S.J. (1999). BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13, 1899–911.Google Scholar
Hao, Y., Lai, L., Mao, J., Im, G.S., Bonk, A. & Prather, R.S. (2003). Apoptosis and in vitro development of preimplantation porcine embryos derived in vitro or by nuclear transfer. Biol. Reprod. 69, 501–7.Google Scholar
Harrington, N.P., Surujballi, O.P., Waters, W.R. & Prescott, J.F. (2007). Development and evaluation of a real-time reverse transcription-PCR assay for quantification of gamma interferon mRNA to diagnose tuberculosis in multiple animal species. Clin. Vaccine Immunol. 14, 1563–71.Google Scholar
Korkmaz, C., Tekin, Y.B., Sakinci, M. & Ercan, C.M. (2015). Effects of maternal ageing on ICSI outcomes and embryo development in relation to oocytes morphological characteristics of birefringent structures. Zygote 23, 550–5.Google Scholar
Lan, G.C., Han, D., Wu, Y.G., Han, Z.B., Ma, S.F., Liu, X.Y., Chang, C.L. & Tan, J.H. (2005). Effects of duration, concentration, and timing of ionomycin and 6-dimethylaminopurine (6-DMAP) treatment on activation of goat oocytes. Mol. Reprod. Dev. 71, 380–8.Google Scholar
Lasiene, K., Vitkus, A., Valanciute, A. & Lasys, V. (2009). Morphological criteria of oocyte quality. Medicina (Kaunas) 45, 509–15.CrossRefGoogle ScholarPubMed
Leroy, J.L., Vanholder, T., Mateusen, B., Christophe, A., Opsomer, G., de Kruif, A., Genicot, G. & Van Soom, A. (2005). Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro . Reproduction 130, 485–95.Google Scholar
Lussier, J.G., Matton, P., Guilbault, L.A., Grasso, F., Mapletoft, R.J. & Carruthers, T.D. (1994). Ovarian follicular development and endocrine responses in follicular-fluid-treated and hemi-ovariectomized heifers. J. Reprod. Fertil. 102, 95–105.CrossRefGoogle ScholarPubMed
Marei, W.F., Wathes, D.C. & Fouladi-Nashta, A.A. (2009). The effect of linolenic acid on bovine oocyte maturation and development. Biol. Reprod. 81, 1064–72.Google Scholar
Marei, W.F., Wathes, D.C. & Fouladi-Nashta, A.A. (2010). Impact of linoleic acid on bovine oocyte maturation and embryo development. Reproduction 139, 979–88.Google Scholar
Marei, W.F., Wathes, D.C. & Fouladi-Nashta, A.A. (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, 679–90.Google Scholar
Mattos, R., Staples, C.R. & Thatcher, W.W. (2000). Effects of dietary fatty acids on reproduction in ruminants. Rev. Reprod. 5, 38–45.CrossRefGoogle ScholarPubMed
McKeegan, P.J. & Sturmey, R.G. (2012). The role of fatty acids in oocyte and early embryo development. Reprod. Fertil. Dev. 24, 59–67.Google Scholar
Mohammadi-Sangcheshmeh, A., Soleimani, M., Deldar, H., Salehi, M., Soudi, S., Hashemi, S.M., Schellander, K. & Hoelker, M. (2011). Prediction of oocyte developmental competence in ovine using glucose-6-phosphate dehydrogenase (G6PDH) activity determined at retrieval time. J. Assist. Reprod. Genet. 29, 153–8.Google Scholar
O’Fallon, J.V., Busboom, J.R., Nelson, M.L. & Gaskins, C.T. (2007). A direct method for fatty acid methyl ester synthesis: application to wet meat tissues, oils, and feedstuffs. J. Anim. Sci. 85, 1511–21.Google Scholar
Ruvolo, P.P., Deng, X. & May, W.S. (2001). Phosphorylation of Bcl2 and regulation of apoptosis. Leukemia 15, 515–22.CrossRefGoogle ScholarPubMed
Santos, J.E., Bilby, T.R., Thatcher, W.W., Staples, C.R. & Silvestre, F.T. (2008). Long chain fatty acids of diet as factors influencing reproduction in cattle. Reprod. Domest. Anim. 43 (Suppl. 2), 23–30.Google Scholar
Song, J.H., Fujimoto, K. & Miyazawa, T. (2000). Polyunsaturated (n-3) fatty acids susceptible to peroxidation are increased in plasma and tissue lipids of rats fed docosahexaenoic acid-containing oils. J. Nutr. 130, 3028–33.CrossRefGoogle ScholarPubMed
Staples, C.R., Burke, J.M. & Thatcher, W.W. (1998). Influence of supplemental fats on reproductive tissues and performance of lactating cows. J. Dairy Sci. 81, 856–71.Google Scholar
Sturmey, R.G., Reis, A., Leese, H.J. & McEvoy, T.G. (2009). Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod. Domest. Anim. 44 (Suppl. 3), 50–8.CrossRefGoogle ScholarPubMed
Thompson, J.G., Gardner, D.K., Pugh, P.A., McMillan, W.H. & Tervit, H.R. (1995). Lamb birth weight is affected by culture system utilized during in vitro pre-elongation development of ovine embryos. Biol. Reprod. 53, 1385–91.Google Scholar
Torres, A., Batista, M., Diniz, P., Silva, E., Mateus, L. & Lopes-da-Costa, L. (2014). Effects of oocyte donor age and embryonic stage of development on transcription of genes coding for enzymes of the prostaglandins and progesterone synthesis pathways in bovine in vitro produced embryos. Zygote 2014, 1–11 DOI: 10.1017/S0967199414000446.Google Scholar
Turathum, B., Saikhun, K., Sangsuwan, P. & Kitiyanant, Y. (2010). Effects of vitrification on nuclear maturation, ultrastructural changes and gene expression of canine oocytes. Reprod. Biol. Endocrinol. 8, 70.Google Scholar
Ulloa, S.M., Heinzmann, J., Herrmann, D., Timmermann, B., Baulain, U., Grossfeld, R., Diederich, M., Lucas-Hahn, A. & Niemann, H. (2015). Effects of different oocyte retrieval and in vitro maturation systems on bovine embryo development and quality. Zygote 23, 367–77.Google ScholarPubMed
Van Hoeck, V., Leroy, J.L., Arias Alvarez, M., Rizos, D., Gutierrez-Adan, A., Schnorbusch, K., Bols, P.E., Leese, H.J. & Sturmey, R.G. (2013). Oocyte developmental failure in response to elevated nonesterified fatty acid concentrations: mechanistic insights. Reproduction 145, 33–44.CrossRefGoogle ScholarPubMed
Veshkini, A., Asadi, H., Khadem, A.A., Mohammadi-Sangcheshmeh, A., Khazabi, S., Aminafshar, M., Deldar, H., Soleimani, M. & Cinar, M.U. (2015). Effect of Linolenic acid during in vitro maturation of ovine oocytes: embryonic developmental potential and mRNA abundances of genes involved in apoptosis. J. Assist. Reprod. Genet. 32, 653–59.CrossRefGoogle ScholarPubMed
Wan, P.C., Hao, Z.D., Zhou, P., Wu, Y., Yang, L., Cui, M.S., Liu, S.R. & Zeng, S.M. (2009). Effects of SOF and CR1 media on developmental competence and cell apoptosis of ovine in vitro fertilization embryos. Anim. Reprod. Sci. 114, 279–88.Google Scholar
Wang, Q. & Sun, Q.Y. (2007). Evaluation of oocyte quality: morphological, cellular and molecular predictors. Reprod. Fertil. Dev. 19, 1–12.Google Scholar
Wonnacott, K.E., Kwong, W.Y., Hughes, J., Salter, A.M., Lea, R.G., Garnsworthy, P.C. & Sinclair, K.D. (2009). Dietary omega-3 and -6 polyunsaturated fatty acids affect the composition and development of sheep granulosa cells, oocytes and embryos. Reproduction 139, 57–69.CrossRefGoogle Scholar