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Interaction between differential gene expression profile and phenotype in bovine blastocysts originating from oocytes exposed to elevated non-esterified fatty acid concentrations

V. Van Hoeck A, D. Rizos B, A. Gutierrez-Adan B, I. Pintelon A, E. Jorssen A, I. Dufort C, M. A. Sirard C, A. Verlaet D, N. Hermans D, P. E. J. Bols A and J. L. M. R. Leroy A E

A Department of Veterinary Sciences, Faculty of Biomedical, Pharmaceutical and Veterinary Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium.
B Departamento de Reproducción Animal y Conservación de Recursos Zoogenéticos, INIA, Ctra. de la Coruna Km 5.9, 28040 Madrid, Spain.
C Département des Sciences Animales Pavillon des services, INAF, Université Laval, G1V 0A6 Québec, Canada.
D Departement Pharmaceutical Sciences, Faculty of Biomedical, Pharmaceutical and Veterinary Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium.
E Corresponding author. Email: jo.leroy@uantwerpen.be

Reproduction, Fertility and Development - http://dx.doi.org/10.1071/RD13263
Submitted: 13 August 2013  Accepted: 28 October 2013   Published online: 23 December 2013


 
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Abstract

Maternal metabolic disorders linked to lipolysis are major risk factors for reproductive failure. A notable feature of such disorders is increased non-esterified fatty acid (NEFA) concentrations in the blood, which are reflected in the ovarian follicular fluid. Elevated NEFA concentrations impact on the maturing oocyte and even alter subsequent embryo physiology. The aetiological mechanisms have not been fully elucidated. Therefore, in the present study, bovine in vitro maturing cumulus–oocyte complexes were exposed (24 h) to three different maturation treatments containing: (1) physiological (72 µM) NEFA concentrations (= control); (2) elevated (75 µM) stearic acid (SA) concentrations (= HIGH SA); and (3) elevated (425 µM) NEFA concentrations (= HIGH COMBI). Zygotes were fertilised and cultured following standard procedures. Transcriptomic analyses in resulting Day 7.5 blastocysts revealed that the major pathways affected are related to lipid and carbohydrate metabolism in HIGH COMBI embryos and to lipid metabolism and cell death in HIGH SA embryos. Furthermore, lower glutathione content and a reduced number of lipid droplets per cell were observed in HIGH SA-exposed oocytes and resulting morulae, respectively, compared with their HIGH COMBI-exposed counterparts. Vitrified embryos originating from HIGH SA-exposed oocytes tended to exhibit lower survival rates compared with controls. These data suggest possible mechanisms explaining why females across species suffering lipolytic disorders experience difficulties in conceiving.

Additional keywords: embryo quality, fertility, lipolysis, maternal metabolism.


References

Aardema, H., Vos, P. L. A. M., Lolicato, F., Roelen, B. A. J., and Knijn, H. M. (2011). Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence. Biol. Reprod. 85, 62–69.
CrossRef | CAS | PubMed |

Aerts, J. M. J., De Clercq, J. B. P., Andries, S., Leroy, J. L. M. R., Van Aelst, S., and Bols, P. E. J. (2008). Follicle survival and growth to antral stages in short-term murine ovarian cortical transplants after Cryologic solid surface vitrification or slow-rate freezing. Cryobiology 57, 163–169.
CrossRef | CAS |

Bermejo-Alvarez, P., Rizos, D., Rath, D., Lonergan, P., and Gutierrez-Adan, A. (2010). Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proc. Natl Acad. Sci. USA 107, 3394–3399.
CrossRef | CAS | PubMed |

Bijttebier, J., Van Soom, A., Meyer, E., Mateusen, B., and Maes, D. (2008). Preovulatory follicular fluid during in vitro maturation decreases polyspermic fertilization of cumulus-intact porcine oocytes: in vitro maturation of porcine oocytes. Theriogenology 70, 715–724.
CrossRef | CAS | PubMed |

Bonnard, C., Durand, A., Peyrol, S., Chanseaume, E., Chauvin, M. A., Morio, B., Vidal, H., and Rieusset, J. (2008). Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J. Clin. Invest. 118, 789–800.
| CAS | PubMed |

Brasaemle, D. L., Rubin, B., Harten, I. A., Gruia-Gray, J., Kimmel, A. R., and Londos, C. (2000). Perilipin A increases triacylglycerol storage by decreasing the rate of triacylglycerol hydrolysis. J. Biol. Chem. 275, 38 486–38 493.
CrossRef | CAS |

Burton, G. J., Hempstock, J., and Jauniaux, E. (2003). Oxygen, early embryonic metabolism and free radical-mediated embryopathies. Reprod. Biomed. Online 6, 84–96.
CrossRef | PubMed |

Cagnone, G. L. M., Dufort, I., Vigneault, C., and Sirard, M. A. (2012). Differential gene expression profile in bovine blastocysts resulting from hyperglycemia exposure during early cleavage stages. Biol. Reprod. 86, 50.
CrossRef |

Carlsson, C., Hakan, B., and Welsh, N. (1999). Sodium palmitate induces partial mitochondrial uncoupling and reactive oxygen species in rat pancreatic islets in vitro. Endocrinology 140, 3422–3428.
CrossRef | CAS | PubMed |

Chavatte-Palmer, P., Al Gubory, K., Picone, O., and Heyman, Y. (2008). Maternal nutrition: effects on offspring fertility and importance of the periconceptional period on long-term development. Gynecol. Obstet. Fertil. 36, 920–929.
CrossRef | CAS | PubMed |

Cnop, M., Hannaert, J. C., Hoorens, A., Eizirik, D. L., and Pipeleers, D. G. (2001). Inverse relationship between cytotoxicity of free fatty acids in pancreatic islet cells and cellular triglyceride accumulation. Diabetes 50, 1771–1777.
CrossRef | CAS | PubMed |

de Matos, D. G., Furnus, C. C., Moses, D. F., and Baldassarre, H. (1995). Effect of cysteamine on glutathione level and developmental capacity of bovine oocyte matured in vitro. Mol. Reprod. Dev. 42, 432–436.
CrossRef | CAS | PubMed |

de Matos, D. G., Furnus, C. C., Moses, D. F., Martinez, A. G., and 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.
CrossRef | CAS | PubMed |

Fedorcsák, P., Storneg, R., Dale, P. O., Tanbo, T., and Abyholm, T. (2000). Obesity is a risk factor for early pregnancy loss after IVF or ICSI. Acta Obstet. Gynecol. Scand. 79, 43–48.
CrossRef | PubMed |

Ferguson, E. M., and Leese, H. J. (1999). Triglyceride content of bovine oocytes and early embryos. J. Reprod. Fertil. 116, 373–378.
CrossRef | CAS | PubMed |

Furukawa, S., Fujita, T., Shimabukuro, M., Iwaki, M., Yamada, Y., Nakajima, Y., Makishima, O., Matsuda, M., and Shimomura, M. (2004). Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Invest. 114, 1752–1761.
| CAS | PubMed |

Geshi, M., Takenouchi, N., Yamauchi, N., and Nagai, T. (2000). Effects of sodium pyruvate in nonserum maturation medium on maturation, fertilization and subsequent development of bovine oocytes with or without cumulus cells. Biol. Reprod. 63, 1730–1734.
CrossRef | CAS | PubMed |

Grupen, C. G., Nagashima, H., and Nottle, M. B. (1995). Cysteamine enhances in vitro development of porcine oocytes matured and fertilized in vitro. Biol. Reprod. 53, 173–178.
CrossRef | CAS | PubMed |

Iossa, S., Mollica, M. P., Lionetti, L., Crescenzo, R., Botta, M., and Liverini, G. (2002). Skeletal muscle oxidative capacity in rats fed high-fat diet. Int. J. Obes. Relat. Metab. Disord. 26, 65–72.
CrossRef | CAS | PubMed |

Jorritsma, R., Cesar, M. L., Hermans, J. T., Kruitwagen, C. L., and Vos, P. L. (2004). Effects of non-esterified fatty acids on bovine granulosa cells and developmental potential of oocytes in vitro. Anim. Reprod. Sci. 81, 225–235.
CrossRef | CAS | PubMed |

Jungheim, E. S., Louden, E. D., Chi, M. M., Frolova, A. I., Riley, J. K., and Moley, K. H. (2011a). Preimplantation exposure of mouse embryos to palmitic acid results in fetal growth restriction followed by catch-up growth in the offspring. Biol. Reprod. 85, 678–683.
CrossRef | CAS | PubMed |

Jungheim, E. S., Macones, G. A., Odem, R. R., Patterson, B. W., Lanzendorf, S. E., Ratts, V. S., and Moley, K. H. (2011b). Associations between free fatty acids, cumulus oocyte complex morphology and ovarian function during in vitro fertilization. Fertil. Steril. 95, 1970–1974.
CrossRef | CAS | PubMed |

Koshkin, V., Wang, X., Scherers, P. E., Chan, C. B., and Wheeler, M. B. (2003). Mitochondrial functional state in clonal pancreatic β cells exposed to free fatty acids. J. Biol. Chem. 278, 19 709–19 715.
CrossRef | CAS |

Latham, K. E., and Sapienza, C. (1998). Localization of genes encoding egg modifiers of paternal genome function to mouse chromosomes one and two. Development 125, 929–935.
| CAS | PubMed |

Leibo, S. P., and Loskutoff, N. M. (1993). Cryobiology of in vitro-derived bovine embryos. Theriogenology 39, 81–94.
CrossRef |

Leroy, J. L., Vanholder, T., Mateusen, B., Christophe, A., and Opsomer, G. (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.
CrossRef | CAS | PubMed |

Leroy, J. L. M. R., Van Soom, A., Opsomer, G., Goovaerts, I. G., and Bols, P. E. (2008). Reduced fertility in high-yielding dairy cows: are the oocyte and embryo in danger? Part II. Mechanisms linking nutrition and reduced oocyte and embryo quality in high-yielding dairy cows. Reprod. Domest. Anim. 43, 623–632.
CrossRef | CAS |

Li, L. O., Klett, E. L., and Coleman, R. A. (2010). Acyl-CoA synthesis, lipid metabolism and lipotoxity. Biochim. Biophys. Acta 1801, 246–251.
CrossRef | CAS | PubMed |

Lu, Z. H., Mu, Y. M., Wang, B. A., Li, X. L., Lu, J. M., Li, J. Y., Pan, C. Y., Yanase, T., and Nawata, H. (2003). Saturated free fatty acids, palmitic acid and stearic acid, induce apoptosis by stimulation of ceramide generation in rat testicular Leydig cell. Biochem. Biophys. Res. Commun. 303, 1002–1007.
CrossRef | CAS | PubMed |

Maedler, K., Spinas, G. A., Dyntar, D., Moritz, W., Kaiser, N., and Donath, M. Y. (2001). Distinct effects of saturated and monounsaturated fatty acids on beta-cell turnover and function. Diabetes 50, 69–76.
CrossRef | CAS | PubMed |

Magielse, J., Verlaet, A., Breynaert, A., Keenoy, B. M. Y., Apers, S., Pieters, L., and Hermans, N. (2013). Investigation of the in vivo antioxidative activity of Cynara scolymus (artichoke) leaf extract. PhD Thesis University of Antwerp.

McGarry, J. D. (2002). Dysregulation of fatty acid metabolism in the etiology of type 2 diabetes. Diabetes 51, 7–18.
CrossRef | CAS | PubMed |

McKeegan, P. J., and Sturmey, R. G. (2012). The role of fatty acids in oocyte and early embryo development. Reprod. Fertil. Dev. 24, 59–67.
CrossRef |

Mohr, L. R., and Trounson, A. O. (1981). Structural changes associated with freezing of bovine embryos. Biol. Reprod. 25, 1009–1025.
CrossRef | CAS | PubMed |

Paczkowski, M., Silva, E., Schoolcraft, W. B., and Krisher, R. L. (2013). Comparative importance of fatty acid beta-oxidation to nuclear maturation, gene expression, and glucose metabolism in mouse, bovine, and porcine cumulus oocyte complexes. Biol. Reprod. 88, 111.
CrossRef | PubMed |

Pasquali, R., Pelusi, C., Genghini, S., Cacciari, M., and Gembineri, A. (2003). Obesity and reproductive disorders in women. Hum. Reprod. Update 9, 359–372.
CrossRef | PubMed |

Perdomo, G., Commerford, S. R., Richard, A. M., Adams, S. H., Corkey, B. E., O’Doherty, R. M., and Brown, N. F. (2004). Increased beta-oxidation in muscle cells enhances insulin-stimulated glucose metabolism and protects against fatty acid-induced insulin resistance despite intramyocellular lipid accumulation. J. Biol. Chem. 279, 27 177–27 186.
CrossRef | CAS |

Quinn, P., and Wales, R. G. (1973). The relationships between the ATP content of preimplantation mouse embryos and their development in vitro during culture. J. Reprod. Fertil. 35, 301–309.
CrossRef | CAS | PubMed |

Reaven, G. M., Hollenbeck, C., Jeng, C. Y., Wu, M. S., and Chen, Y. D. (1988). Measurement of plasma glucose, free fatty acid, and insulin for 24 h in patients with NIDDM. Diabetes 37, 1020–1024.
CrossRef | CAS | PubMed |

Robker, R. L., Akison, L. K., Bennett, B. D., Thrupp, P. N., Chura, L. R., Russell, D. L., Lane, M., and Norman, R. J. (2009). Obese women exhibit differences in ovarian metabolites, hormones, and gene expression compared with moderate-weight women. J. Clin. Endocrinol. Metab. 94, 1533–1540.
CrossRef | CAS | PubMed |

Schmittgen, T. D., and Livak, K. J. (2008). Analysing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101–1108.
CrossRef | CAS | PubMed |

Shimabukuro, M., Ohneda, M., Lee, Y., and Unger, R. H. (1997). Role of nitric oxide in obesity-induced beta cell disease. J. Clin. Invest. 100, 290–295.
CrossRef | CAS | PubMed |

Shimabukuro, M., Zhou, Y. T., Levi, M., and Unger, R. H. (1998). Fatty acid-induced β-cell apoptosis: a link between obesity and diabetes. Proc. Natl Acad. Sci. USA 95, 2498–2502.
CrossRef | CAS | PubMed |

Štolba, P., Kvapil, M., Wichterle, D., and Dvořák, P. (1993). Kinetics of free fatty acids in hypertriglyceridemia. Evidence for different types of insulin resistance. Ann. N. Y. Acad. Sci. 683, 373–375.
CrossRef | PubMed |

Souza, S. C., Muliro, K. V., Liscum, L., Lien, P., Yamamoto, M. T., Schaffer, J. E., Dallal, G. E., Wang, X., Kraemer, F. B., Obin, M., and Greenberg, A. S. (2002). Modulation of hormone-sensitive lipase and protein kinase A-mediated lipolysis by perilipin A in an adenoviral reconstituted system. J. Biol. Chem. 277, 8267–8272.
CrossRef | CAS | PubMed |

Sutton-McDowall, M. L., Gilchrist, R. B., and Thompson, J. G. (2004). Cumulus expansion and glucose utilisation by bovine cumulus–oocyte complexes during in vitro maturation: the influence of glucosamine and follicle-stimulating hormone. Reproduction 128, 313–319.
CrossRef | CAS | PubMed |

Tanghe, S., Van Soom, A., Nauwynck, H., Coryn, M., and de Kruif, A. (2002). Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol. Reprod. Dev. 61, 414–424.
CrossRef | CAS | PubMed |

Tarín, J. J. (1996). Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Mol. Hum. Reprod. 2, 717–724.
CrossRef | PubMed |

Ulloth, J. E., Casiano, C. A., and De Leon, M. (2003). Palmitic and stearic fatty acids induce caspase-dependent and -independent cell death in nerve growth factor differentiated PC12 cells. J. Neurochem. 84, 655–668.
CrossRef | CAS | PubMed |

Vajta, G., Holm, P., Kuwayama, M., Booth, P. J., Jacobsen, H., Greve, T., and Callesen, H. (1998). Open pulled straw (OPS) vitrification: a new way to reduce cryoinjuries of bovine ova and embryos. Mol. Reprod. Dev. 51, 53–58.
CrossRef | CAS | PubMed |

Valckx, S., Bols, P. E. J., De Neubourg, D., Berth, M., De Pauw, I., and Leroy, J. L. M. R. (2010). Maternal metabolism and the influence on fertility: a study of the follicular environment. In ‘Proceedings of the 3rd Meeting of Gemini, Soustons, France, 1–3 October 2010.’ Available at http://www.cost-gemini.eu/ISBN%20Productions%20(electronic%20copy)/9780956369451_GEMINI_Programme_Booklet_1_3_Oct_2010.pdf

Van Blerkom, J., Davis, P. W., and Lee, J. (1995). ATP content of human oocytes and developmental potential and outcome after in vitro fertilization and embryo transfer. Hum. Reprod. 10, 415–424.
| CAS | PubMed |

Van Hoeck, V., Sturmey, R. G., Bermejo-Alvarez, P., Rizos, D., Gutierrez-Adan, A., Leese, H. J., Bols, P. E. J., and Leroy, J. L. M. R. (2011). Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology. PLoS One 6, e23183.
CrossRef | CAS | PubMed |

Van Hoeck, V., Leroy, J. L. M. R., Arias-Álvarez, M., Rizos, D., Gutierrez-Adan, A., Schnorbusch, K., Bols, P. E. J., Leese, H. J., and Sturmey, R. G. S. (2013). Oocyte developmental failure in response to elevated non-esterified fatty acid concentrations: mechanistic insights. Reproduction 145, 33–44.
CrossRef | CAS | PubMed |

Vanholder, T., Leroy, J. L., Van Soom, A., Opsomer, G., Maes, D., Coryn, M., and de Kruif, A. (2005). Effect of non-esterified fatty acids on bovine granulosa cell steroidogenesis and proliferation in vitro. Anim. Reprod. Sci. 87, 33–44.
CrossRef | CAS | PubMed |

Watkins, A. J., Wilkins, A., Cunningham, C., Perry, V. H., Seet, M. J., Osmond, C., Eckert, J. J., Torrens, C., Cagampang, F. R. A., Cleal, J., Gray, W. P., Hanson, M. A., and Fleming, T. P. (2008). Low protein diet fed exclusively during mouse oocyte maturation leads to behavioural and cardiovascular abnormalities in offspring. J. Physiol. 586, 2231–2244.
CrossRef | CAS | PubMed |

Wu, D., and Cederbaum, A. (2000). Ethanol and arachidonic acid produce toxicity in hepatocytes from pyrazole-treated rats with high levels of CYP2E1. Mol. Cell. Biochem. 204, 157–167.
CrossRef | CAS | PubMed |

Zhang, X., and Zhang, K. (2012). Endoplasmic reticulum stress-associated lipid droplet formation and type II diabetes. Biochem. Res. Int. 2012, Article ID 247275.
CrossRef |

Zhang, W. Y., Schwartz, E., Wang, Y., Atrep, J., Li, Z., and Reaven, P. (2006). Elevated concentrations of nonesterified fatty acids increase monocyte expression of CD11b and adhesion to endothelial cells. Arterioscler. Thromb. Vasc. Biol. 26, 514–519.
CrossRef | CAS | PubMed |


   
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