Vet Med - Czech, 2011, 56(4):156-167 | DOI: 10.17221/1573-VETMED
Maternal nutrition affects the composition of follicular fluid and transcript content in gilt oocytes
- Faculty of Animal Breeding and Biology, Poznan University of Life Sciences, Poznan, Poland
Metabolomics focused on reproduction have been the subject of special interest in the past decade. Metabolite profiling provides detailed information on the status of follicular fluid and follicular cells which accompany the growing oocyte. Although nutrients present in the diet reach oocytes via the follicular fluid, it is not evident whether oocyte/embryo quality can be predicted based on the follicular fluid composition. Since this phenomenon has not yet been investigated in the pig, the aim of the present study was to investigate associations between diet composition and (1) selected markers related to developmental potential of oocytes (brilliant cresyl blue - BCB test, relative transcript abundance of EEF1A1 and ATP5A1 marker genes) and (2) fatty acid profile in the follicular fluid. Gilts were fed control and experimental diets which differed in composition and fatty acid profiles. The experimental diet used in this study comprised mainly locally grown grains (barley and rye) traditionally used for fattening pigs in Poland. Cumulus-oocyte complexes were aspirated from individual pairs of ovaries after animal slaughter, evaluated morphologically and subjected to the BCB test. Relative transcript abundance for the two marker genes was monitored by real-time PCR in oocytes of both categories (BCB+ and BCB-). Fatty acid profile in follicular fluid was analyzed by gas chromatography. We show that the experimental diet rich in n-3 fatty acid significantly influences fatty acid composition of the follicular fluid. The fatty acid profile of the follicular fluid of gilts fed the experimental diet differed from that of the control females. The content of saturated fatty acids was higher in the experimental group, whereas unsaturated and polyunsaturated fatty acids were more abundant in the control group (P < 0.05). With regard to individual fatty acids, only C16:0 (palmitic acid), C18:2n-6 (linoleic acid) and C22:6 (docosahexaenoic acid) differed significantly. The abundance of ATP5A1 mRNA was influenced neither by diet composition nor by oocyte category (BCB+/BCB-) whereas that of the EEF1A1 was affected by both factors. Since higher mRNA level of the EEF1A1 gene was noted in BCB+ oocytes this may be considered as a marker of oocyte quality in the pig.
Keywords: fatty acids; BCB test; pig; EEF1A1; ATP5A1
Published: April 30, 2011 Show citation
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References
- Abayasekara DR, Wathes DC (1999): Effects of altering dietary fatty acid composition on prostaglandin synthesis and fertility. Prostaglandins, Leukotrienes and Essential Fatty Acids 61, 275-287.
Go to original source...
Go to PubMed...
- Alm H, Torner H, Lohrke B, Viergutz T, Ghoneim IM, Kanitz W (2005): Bovine blastocyst development rate in vitro is influenced by selection of oocytes by brilliant cresyl blue staining before IVM as indicator for glucose-6-phosphate dehydrogenase activity. Theriogenology 63, 2194-2205.
Go to original source...
Go to PubMed...
- Association of Official Analytical Chemists, AOAC (2006): Official Methods of Analysis. 18th ed. W. Horowitz W and W. Latimer W, Gaithersburg Maryland, USA.
- Bilby TR, Block J, do Amaral BC, Sa Filho O, Silvestre FT, Hansen PJ, Staples CR, Thatcher WW (2006): Effects of dietary unsaturated fatty acids on oocyte quality and follicular development in lactating dairy cows in summer. Journal of Dairy Science 89, 3891-3903.
Go to original source...
Go to PubMed...
- Boland MP, Lonergan P, O'Callaghan D (2001): Effect of nutrition on endocrine parameters, ovarian physiology, and oocyte and embryo development. Theriogenology 55, 1323-1340.
Go to original source...
Go to PubMed...
- Booth PJ, Humpherson PG, Watson TJ, Leese HJ (2005): Amino acid depletion and appearance during porcine preimplantation embryo development in vitro. Reproduction 130, 655-668.
Go to original source...
Go to PubMed...
- Brevini-Gandolfi TA, Favetta LA, Mauri L, Luciano AM, Cillo F, Gandolfi F (1999): Changes in poly(A) tail length of maternal transcripts during in vitro maturation of bovine oocytes and their relation with developmental competence. Molecular Reproduction and Development 52, 427-433.
Go to original source...
Go to PubMed...
- Cerri RL, Juchem SO, Chebel RC, Rutigliano HM, Bruno RG, Galvao KN, Thatcher WW, Santos JE (2009): Effect of fat source differing in fatty acid profile on metabolic parameters, fertilization, and embryo quality in highproducing dairy cows. Journal of Dairy Science 92, 1520-1531.
Go to original source...
Go to PubMed...
- Cieslak A, Machmuller A, Szumacher-Strabel M, Scheeder MRL (2009): A comparison of two extraction methods used to quantify the C18 fatty acids in feed and digesta of ruminants. Journal of Animal Feed Sciences 18, 362-367.
Go to original source...
- El Shourbagy SH, Spikings EC, Freitas M, St John JC (2006): Mitochondria directly influence fertilisation outcome in the pig. Reproduction 131, 233-245.
Go to original source...
Go to PubMed...
- Fouladi-Nashta AA, Gutierrez CG, Gong JG, Garnsworthy PC, Webb R (2007): Impact of dietary fatty acids on oocyte quality and development in lactating dairy cows. Biology of Reproduction 77, 9-17.
Go to original source...
Go to PubMed...
- Goossens K, Van Soom A, Van Poucke M, Vandaele L, Vandesompele J, Van Zeveren A, Peelman LJ (2007): Identification and expression analysis of genes associated with bovine blastocyst formation. BMC Developmental Biology 7, 64.
Go to original source...
Go to PubMed...
- Homa ST, Brown CA (1992): Changes in linoleic acid during follicular development and inhibition of spontaneous breakdown of germinal vesicles in cumulusfree bovine oocytes. Journal of Reproduction and Fertility 94, 153-160.
Go to original source...
Go to PubMed...
- Ishizaki C, Watanabe H, Bhuiyan MM, Fukui Y (2009): Developmental competence of porcine oocytes selected by brilliant cresyl blue and matured individually in a chemically defined culture medium. Theriogenology 72, 72-80.
Go to original source...
Go to PubMed...
- Kendrick KW, Bailey TL, Garst AS, Pryor AW, Ahmadzadeh A, Akers RM, Eyestone WE, Pearson RE, Gwazdauskas FC (1999): Effects of energy balance of hormones, ovarian activity, and recovered oocytes in lactating Holstein cows using transvaginal follicular aspiration. Journal of Dairy Science 82 1731- 1741.
Go to original source...
Go to PubMed...
- Kojima T, Zeniya Y, Auyama T, Kondo A, Yoshino J (1997): Dietary administration of fatty acids-enriched mold dried cell containing γ-linolenic acid to female pigs improves ovulation rate and embryo quality in summer. Journal of Reproduction and Development 43, 121-127.
Go to original source...
- Krisher RL (2004): The effect of oocyte quality on development. Journal of Animal Science 82 (E-Suppl.), E14-E23.
Go to PubMed...
- Leroy JL, 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, 485-495.
Go to original source...
Go to PubMed...
- Madeja ZE, Warzych E, Peippo J, Lechniak D, Switonski M (2009): Gene expression and protein distribution of leptin and its receptor in bovine oocytes and preattachment embryos produced in vitro. Animal 3, 568-578.
Go to original source...
Go to PubMed...
- Marei WF, Wathes DC, Fouladi-Nashta AA (2009): The effect of linolenic acid on bovine oocyte maturation and development. Biology of Reproduction 81, 1064- 1072.
Go to original source...
Go to PubMed...
- McEvoy TG, Coull GD, Broadbent PJ, Hutchinson JSM, Speake BK (2000): Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. Journal of Reproduction and Fertility 118, 163-170.
Go to original source...
- Moldave K (1985): Eukaryotic protein synthesis. Annual Review of Biochemistry 54, 1109-1149.
Go to original source...
Go to PubMed...
- Nonogaki T, Noda Y, Goto Y, Kishi J, Mori T (1994): Developmental blockage of mouse embryos caused by fatty acids. Journal of Assisted Reproduction and Genetics 11, 482-488.
Go to original source...
Go to PubMed...
- Pedersen PL (1994): ATP synthase. The machine that makes ATP. Current Biology 4, 1138-1141.
Go to original source...
Go to PubMed...
- Pike IH, Barlow SM (2000): The fats of life - the role of fish. Lipid Technology 13, 58-60.
- Pisani LF, Antonini S, Pocar P, Ferrari S, Brevini TA, Rhind SM, Gandolfi F (2008): Effects of pre-mating nutrition on mRNA levels of developmentally relevant genes in sheep oocytes and granulosa cells. Reproduction 136, 303-312.
Go to original source...
Go to PubMed...
- Preis KA, Seidel G Jr, Gardner DK (2005): Metabolic markers of developmental competence for in vitro matured mouse oocytes. Reproduction 130, 475-483.
Go to original source...
Go to PubMed...
- Racedo SE, Wrenzycki C, Lepikhov K, Salamone D, Walter J, Niemann H (2009): Epigenetic modifications and related mRNA expression during bovine oocyte in vitro maturation. Reproduction Fertility and Development 21, 738-748.
Go to original source...
Go to PubMed...
- Renaville B, Bacciu N, Comin A, Motta M, Poli I, Vanini G, Prandi A (2010): Plasma and follicular fluid fatty acid profiles in dairy cows. Reproduction in Domestic Animals 45, 118-121.
Go to original source...
Go to PubMed...
- Revelli A, Delle Piane L, Casano S, Molinari E, Massobrio M, Rinaudo P (2009): Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics. Reproductive Biology and Endocrinology 7, 40.
Go to original source...
Go to PubMed...
- Roca J, Martinez E, Vazquez JM, Lucas X (1998): Selection of immature pig oocytes for homologous in vitro penetration assays with the brilliant cresyl blue test. Reproduction Fertility and Development 10, 479-485.
Go to original source...
Go to PubMed...
- Rodriguez-Gonzalez E, Lopez-Bejar M, Izquierdo D, Paramio MT (2003): Developmental competence of prepubertal goat oocytes selected with brilliant cresyl blue and matured with cysteamine supplementation. Reproduction Nutrition and Development 43, 179-187.
Go to original source...
Go to PubMed...
- Santos JEP, Bilby TR, Thatcher WW, Stalpes CR, Silvestre FT (2008): Long chain fatty acids of diet as factors influencing reproduction in cattle. Reproduction in Domestic Animals 43 (Suppl. 2), 23-30.
Go to original source...
Go to PubMed...
- Shehab-El-Deen MA, Leroy JL, Maes D, Van Soom A (2009): Cryotolerance of bovine blastocysts is affected by oocyte maturation in media containing palmitic or stearic acid. Reproduction in Domestic Animals 44, 140-142.
Go to original source...
Go to PubMed...
- Sinclair KD, Lunn LA, Kwong WY, Wonnacott K, Linforth RS, Craigon J (2008): Amino acid and fatty acid composition of follicular fluid as predictors of in-vitro embryo development. Reproductive Biomedicine Online 16, 859-868.
Go to original source...
Go to PubMed...
- Sirard MA, Richard F, Blondin P, Robert C (2006): Contribution of the oocyte to embryo quality. Theriogenology 65, 126-136.
Go to original source...
Go to PubMed...
- Sturmey RG, Reis A, Leese HJ, McEvoy TG (2009): Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reproduction in Domestic Animals 44 (Suppl. 3), 50-58.
Go to original source...
Go to PubMed...
- Torner H, Ghanem N, Ambros C, Holker M, Tomek W, Phatsara C, Alm H, Sirard MA, Kanitz W, Schellander K, Tesfaye D (2008): Molecular and subcellular characterisation of oocytes screened for their developmental competence based on glucose-6-phosphate dehydrogenase activity. Reproduction 135, 197-212.
Go to original source...
Go to PubMed...
- Wakefield SL, Lane M, Schulz SJ, Hebart ML, Thompson JG, Mitchell M (2008): Maternal supply of omega-3 polyunsaturated fatty acids alter mechanisms involved in oocyte and early embryo development in the mouse. American Journal of Physiology, Endocrinology and Metabolism 294, E425-E434.
Go to original source...
Go to PubMed...
- Wathes DC, Abayasekara DR, Aitken RJ (2007): Polyunsaturated fatty acids in male and female reproduction. Biology of Reproduction 77, 190-201.
Go to original source...
Go to PubMed...
- Wongsrikeao P, Otoi T, Yamasaki H, Agung B, Taniguchi M, Naoi H, Shimizu R, Nagai T (2006): Effects of single and double exposure to brilliant cresyl blue on the selection of porcine oocytes for in vitro production of embryos. Theriogenology 66, 366-372.
Go to original source...
Go to PubMed...
- Wonnacott KE, Kwong WY, Hughes J, Salter AM, Lea RG, Garnsworthy PC, Sinclair KD (2010): Dietary omega-3 and -6 polyunsaturated fatty acids affect the composition and development of sheep granulosa cells, oocytes and embryos. Reproduction 139, 57-69.
Go to original source...
Go to PubMed...
- Wrenzycki C, De Sousa P, Overstrom EW, Duby RT, Herrmann D, Watson AJ, Niemann H, O'Callaghan D, Boland MP (2000): Effects of superovulated heifer diet type and quantity on relative mRNA abundances and pyruvate metabolism in recovered embryos. Journal of Reproduction and Fertility 118, 69-78.
Go to original source...
- Wu YG, Liu Y, Zhou P, Lan GC, Han D, Miao DQ, Tan JH (2007): Selection of oocytes for in vitro maturation by brilliant cresyl blue staining: a study using the mouse model. Cell Research 17, 722-731.
Go to original source...
Go to PubMed...
- Yotov WV, St-Arnaud R (1993): Cloning and functional expression analysis of the alpha subunit of mouse ATP synthase. Biochemical and Biophysical Research Communications 191, 142-148.
Go to original source...
Go to PubMed...
- Zak LJ, Xu X, Hardin RT, Foxcroft GR (1997): Impact of different patterns of feed intake during lactation in the primiparous sow on follicular development and oocyte maturation. Journal of Reproduction and Fertility 110, 99-106.
Go to original source...
Go to PubMed...
- Zeron Y, Ocheretny A, Kedar O, Borochov A, Sklan D, Arav A (2001): Seasonal changes in bovine fertility: relation to developmental competence of oocytes, membrane properties and fatty acid composition of follicles. Reproduction 121, 447-454.
Go to original source...
Go to PubMed...
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