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The effect of nutrition and metabolic status on the development of follicles, oocytes and embryos in ruminants

Published online by Cambridge University Press:  28 April 2014

J. Dupont ,
R. J. Scaramuzzi  and
M. Reverchon
J. Dupont*
Affiliation:
INRA, UMR85 Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France CNRS, UMR6175 Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France Université François Rabelais de Tours, F-37041 Tours, France IFCE, F-37380 Nouzilly, France
R. J. Scaramuzzi
Affiliation:
INRA, UMR85 Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France Department of Comparative Biomedical Sciences, The Royal Veterinary College, Hawkshead Lane, North Mimms, Hertfordshire AL9 7TA, UK
M. Reverchon
Affiliation:
INRA, UMR85 Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France CNRS, UMR6175 Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France Université François Rabelais de Tours, F-37041 Tours, France IFCE, F-37380 Nouzilly, France
*
†E-mail: [email protected]
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Abstract

The impact of nutrition and energy reserves on the fertility of ruminants has been extensively described. However, the metabolic factors and the molecular mechanisms involved in the interactions between nutrition and ovarian function are still poorly understood. These factors could be hormonal (either reproductive and/or metabolic) and/or dietary and metabolic (glucose, amino acids and fatty acids). In this review, we briefly summarize the impact of those nutrients (fatty acids, glucose and amino acids) and metabolic hormones (insulin/IGF-I, growth hormone, T3/4, ghrelin, apelin and the adipokines (leptin, adiponectin and resistin)) implicated in the development of ovarian follicles, oocytes and embryos in ruminants. We then discuss the current hypotheses on the mechanisms of action of these factors on ovarian function. We particularly describe the role of some energy sensors including adenosine monophosphate-activated kinase and peroxisome proliferator-activated receptors in the ovarian cells.

Keywords

nutrientsmetabolic hormonesovarymechanism of actionruminant
Type
Full Paper
Information
animal , Volume 8 , Issue 7 , July 2014 , pp. 1031 - 1044
Copyright
© The Animal Consortium 2014 

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References

Aardema, H, Vos, PL, Lolicato, F, Roelen, BA, Knijn, HM, Vaandrager, AB, Helms, JB and Gadella, BM 2011. Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence. Biology of Reproduction 85, 62–69.Google Scholar
Aardema, H, Lolicato, F, van de Lest, CH, Brouwers, JF, Vaandrager, AB, van Tol, HT, Roelen, BA, Vos, PL, Helms, JB and Gadella, BM 2013. Bovine cumulus cells protect maturing oocytes from increased fatty acid levels by massive intracellular lipid storage. Biology of Reproduction 88, 164.CrossRefGoogle ScholarPubMed
Ambrose, DJ, Kastelic, JP, Corbett, R, Pitney, PA, Petit, HV, Small, JA and Zalkovic, P 2006. Lower pregnancy losses in lactating dairy cows fed a diet enriched in alpha-linolenic acid. Journal of Dairy Science 89, 3066–3074.CrossRefGoogle ScholarPubMed
Armstrong, DG, Gutierrez, CG, Baxter, G, Glazyrin, AL, Mann, GE, Woad, KJ, Hogg, CO and Webb, R 2000. Expression of mRNA encoding IGF-I, IGF-II and type 1 IGF receptor in bovine ovarian follicles. Journal of Endocrinology 165, 101–113.Google Scholar
Ashkar, FA, Semple, E, Schmidt, CH St, John, E, Bartlewski, PM and King, WA 2010. Thyroid hormone supplementation improves bovine embryo development in vitro. Human Reproduction 25, 334–344.CrossRefGoogle ScholarPubMed
Bai, R, Zhao, P, Cao, G, Wen, S, Li, Q and Meng, Q 2012. Ghrelin promotion of oocyte maturation via ERK1/2 pathway in ovis aries. Cellular and Molecular Biology (Noisy-le-grand) 58 (suppl.), OL1797–OL1802.Google Scholar
Beam, SW and Butler, WR 1998. Energy balance, metabolic hormones, and early postpartum follicular development in dairy cows fed prilled lipid. Journal of Dairy Science 81, 121–131.CrossRefGoogle ScholarPubMed
Beam, SW and Butler, WR 1999. Effects of energy balance on follicular development and first ovulation in postpartum dairy cows. Journal of Reproduction and Fertility Supplement 54, 411–424.Google Scholar
Berger, J and Moller, DE 2002. The mechanisms of action of PPARs. Annual Review of Medicine 53, 409–435.Google Scholar
Berlinguer, F, Gonzalez-Bulnes, A, Contreras-Solis, I, Spezzigu, A, Torres-Rovira, L, Succu, S, Naitana, S and Leoni, GG 2012. Glucogenic supply increases oocyte developmental competence in sheep. Reproduction, Fertility and Development 24, 1055–1062.Google Scholar
Bernal, A, DeMoraes, GV, Thrift, TA, Willard, CC and Randel, RD 1999. Effects of induced hypothyroidism on ovarian response to superovulation in Brahman (Bos indicus) cows. Journal of Animal Science 77, 2749–2756.Google Scholar
Bilby, TR, Block, J, do Amaral, BC, Sa Filho, O, Silvestre, FT, Hansen, PJ, Staples, CR and 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.Google Scholar
Bilodeau-Goeseels, S 2006. Effects of culture media and energy sources on the inhibition of nuclear maturation in bovine oocytes. Theriogenology 66, 297–306.CrossRefGoogle ScholarPubMed
Bilodeau-Goeseels, S 2011. Cows are not mice: the role of cyclic AMP, phosphodiesterases, and adenosine monophosphate-activated protein kinase in the maintenance of meiotic arrest in bovine oocytes. Molecular Reproduction and Development 78, 734–743.CrossRefGoogle Scholar
Bilodeau-Goeseels, S, Sasseville, M, Guillemette, C and Richard, FJ 2007. Effects of adenosine monophosphate-activated kinase activators on bovine oocyte nuclear maturation in vitro. Molecular Reproduction and Development 74, 1021–1034.CrossRefGoogle ScholarPubMed
Boelhauve, M, Sinowatz, F, Wolf, E and Paula-Lopes, FF 2005. Maturation of bovine oocytes in the presence of leptin improves development and reduces apoptosis of in vitro-produced blastocysts. Biology of Reproduction 73, 737–744.Google Scholar
Boland, MP, Lonergan, P and O'Callaghan, D 2001. Effect of nutrition on endocrine parameters, ovarian physiology, and oocyte and embryo development. Theriogenology 55, 1323–1340.Google Scholar
Boucher, J, Masri, B, Daviaud, D, Gesta, S, Guigne, C, Mazzucotelli, A, Castan-Laurell, I, Tack, I, Knibiehler, B, Carpene, C, Audigier, Y, Saulnier-Blache, JS and Valet, P 2005. Apelin, a newly identified adipokine up-regulated by insulin and obesity. Endocrinology 146, 1764–1771.Google Scholar
Bradford, BJ and Allen, MS 2008. Negative energy balance increases periprandial ghrelin and growth hormone concentrations in lactating dairy cows. Domestic Animal Endocrinology 34, 196–203.CrossRefGoogle ScholarPubMed
Braw-Tal, R, Pen, S and Roth, Z 2009. Ovarian cysts in high-yielding dairy cows. Theriogenology 72, 690–698.CrossRefGoogle ScholarPubMed
Butler, WR 2003. Energy balance relationships with follicular development, ovulation and fertility in postpartum dairy cows. Livestock Production Science 83, 211–218.Google Scholar
Byrne, AT, Southgate, J, Brison, DR and Leese, HJ 2002. Regulation of apoptosis in the bovine blastocyst by insulin and the insulin-like growth factor (IGF) superfamily. Molecular Reproduction and Development 62, 489–495.Google Scholar
Cetica, P, Pintos, L, Dalvit, G and Beconi, M 2002. Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro. Reproduction 124, 675–681.Google Scholar
Childs, S, Hennessy, AA, Sreenan, JM, Wathes, DC, Cheng, Z, Stanton, C, Diskin, MG and Kenny, DA 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
Ciccioli, NH, Wettemann, RP, Spicer, LJ, Lents, CA, White, FJ and Keisler, DH 2003. Influence of body condition at calving and postpartum nutrition on endocrine function and reproductive performance of primiparous beef cows. Journal of Animal Science 81, 3107–3120.Google Scholar
Collado-Fernandez, E, Picton, HM and Dumollard, R 2012. Metabolism throughout follicle and oocyte development in mammals. International Journal of Developmental Biology 56, 799–808.CrossRefGoogle ScholarPubMed
Cordova, B, Morato, R, de Frutos, C, Bermejo-Alvarez, P, Paramio, T, Gutierrez-Adan, A and Mogas, T 2011. Effect of leptin during in vitro maturation of prepubertal calf oocytes: embryonic development and relative mRNA abundances of genes involved in apoptosis and oocyte competence. Theriogenology 76, 1706–1715.Google Scholar
Costa, NN, Cordeiro, MS, Silva, TV, Sastre, D, Santana, PP, Sa, AL, Sampaio, RV, Santos, SS, Adona, PR, Miranda, MS and Ohashi, OM 2013. Effect of triiodothyronine on developmental competence of bovine oocytes. Theriogenology 80, 295–301.Google Scholar
Cui, Y, Miyoshi, K, Claudio, E, Siebenlist, UK, Gonzalez, FJ, Flaws, J, Wagner, KU and Hennighausen, L 2002. Loss of the peroxisome proliferation-activated receptor gamma (PPARgamma) does not affect mammary development and propensity for tumor formation but leads to reduced fertility. Journal of Biological Chemistry 277, 17830–17835.CrossRefGoogle Scholar
Dayi, A, Bediz, CS, Musal, B, Yilmaz, O, Comlekci, A, Celiloglu, M and Cimrin, D 2005. Comparison of leptin levels in serum and follicular fluid during the oestrous cycle in cows. Acta Veterinaria Hungarica 53, 457–467.Google Scholar
de Prada, JK and VandeVoort, CA 2008. Growth hormone and in vitro maturation of rhesus macaque oocytes and subsequent embryo development. Journal of Assisted Reproduction and Genetics 25, 145–158.Google Scholar
Deaver, SE, Hoyer, PB, Dial, SM, Field, ME, Collier, RJ and Rhoads, ML 2013. Localization of ghrelin and its receptor in the reproductive tract of Holstein heifers. Journal of Dairy Science 96, 150–157.Google Scholar
Delavaud, C, Bocquier, F, Chilliard, Y, Keisler, DH, Gertler, A and Kann, G 2000. Plasma leptin determination in ruminants: effect of nutritional status and body fatness on plasma leptin concentration assessed by a specific RIA in sheep. Journal of Endocrinology 165, 519–526.Google Scholar
Delavaud, C, Ferlay, A, Faulconnier, Y, Bocquier, F, Kann, G and Chilliard, Y 2002. Plasma leptin concentration in adult cattle: effects of breed, adiposity, feeding level, and meal intake. Journal of Animal Science 80, 1317–1328.Google Scholar
Diskin, MG, Mackey, DR, Roche, JF and Sreenan, JM 2003. Effects of nutrition and metabolic status on circulating hormones and ovarian follicle development in cattle. Animal Reproduction Science 78, 345–370.Google Scholar
Downie, JG and Gelman, AL 1976. The relationship between changes in bodyweight plasma glucose and fertility in beef cows. Veterinary Record 99, 210–212.CrossRefGoogle ScholarPubMed
Downing, JA and Scaramuzzi, RJ 1991. Nutrient effects on ovulation rate, ovarian function and the secretion of gonadotrophic and metabolic hormones in sheep. Journal of Reproduction and Fertility Supplement 43, 209–227.Google ScholarPubMed
Downing, JA, Joss, J and Scaramuzzi, RJ 1995. A mixture of the branched chain amino acids leucine, isoleucine and valine increases ovulation rate in ewes when infused during the late luteal phase of the oestrous cycle: an effect that may be mediated by insulin. Journal of Endocrinology 145, 315–323.Google Scholar
Downing, JA, Joss, J and Scaramuzzi, RJ 1999. The effect of a direct arterial infusion of insulin and glucose on the ovarian secretion rates of androstenedione and oestradiol in ewes with an autotransplanted ovary. Journal of Endocrinology 163, 531–541.Google Scholar
Downs, SM and Chen, J 2006. Induction of meiotic maturation in mouse oocytes by adenosine analogs. Molecular Reproduction and Development 73, 1159–1168.Google Scholar
Downs, SM, Mosey, JL and Klinger, J 2009. Fatty acid oxidation and meiotic resumption in mouse oocytes. Molecular Reproduction and Development 76, 844–853.Google Scholar
Du, C, Li, H, Cao, G, Xilingaowa, , Wang, C and Li, C 2010. Expression of the orexigenic peptide ghrelin and the type 1a growth hormone secretagogue receptor in sheep oocytes and pre-implantation embryos produced in vitro. Reproduction in Domestic Animals 45, 92–98.Google Scholar
Du, C, Xilingaowa, , Cao, G, Wang, C, Li, H, Zhao, Y, Siqingaowa, and Cao, J 2009. Expression of the orexigenic peptide ghrelin in the sheep ovary. Domestic Animal Endocrinology 36, 89–98.Google Scholar
Dunning, KR, Cashman, K, Russell, DL, Thompson, JG, Norman, RJ and Robker, RL 2010. Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development. Biology of Reproduction 83, 909–918.CrossRefGoogle ScholarPubMed
Dupont, J and LeRoith, D 2001. Insulin and insulin-like growth factor I receptors: similarities and differences in signal transduction. Hormone Research 55 (suppl. 2), 22–26.Google Scholar
Dupont, J, Chabrolle, C, Rame, C, Tosca, L and Coyral-Castel, S 2008. Role of the peroxisome proliferator-activated receptors, adenosine monophosphate-activated kinase, and adiponectin in the ovary. PPAR Research 2008, 176275.Google Scholar
Einspanier, R, Miyamoto, A, Schams, D, Muller, M and Brem, G 1990. Tissue concentration, mRNA expression and stimulation of IGF-I in luteal tissue during the oestrous cycle and pregnancy of cows. Journal of Reproduction and Fertility 90, 439–445.CrossRefGoogle ScholarPubMed
Eppig, JJ 1976. Analysis of mouse oogenesis in vitro. Oocyte isolation and the utilization of exogenous energy sources by growing oocytes. Journal of Experimental Zoology 198, 375–382.CrossRefGoogle ScholarPubMed
Ferguson, EM and Leese, HJ 1999. Triglyceride content of bovine oocytes and early embryos. Journal of Reproduction and Fertility 116, 373–378.Google Scholar
Forman, BM, Chen, J and Evans, RM 1997. Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors alpha and delta. Proceedings of the National Academy of Sciences of the United States of America 94, 4312–4317.Google Scholar
Fouladi-Nashta, AA, Gutierrez, CG, Gong, JG, Garnsworthy, PC and Webb, R 2007. Impact of dietary fatty acids on oocyte quality and development in lactating dairy cows. Biology of Reproduction 77, 9–17.Google Scholar
Froment, P, Fabre, S, Dupont, J, Pisselet, C, Chesneau, D, Staels, B and Monget, P 2003. Expression and functional role of peroxisome proliferator-activated receptor-gamma in ovarian folliculogenesis in the sheep. Biology of Reproduction 69, 1665–1674.Google Scholar
Gallet, C, Dupont, J, Campbell, BK, Monniaux, D, Guillaume, D and Scaramuzzi, RJ 2011. The infusion of glucose in ewes during the luteal phase increases the number of follicles but reduces oestradiol production and some correlates of metabolic function in the large follicles. Animal Reproduction Science 127, 154–163.Google Scholar
Garnsworthy, PC, Gong, JG, Armstrong, DG, Newbold, JR, Marsden, M, Richards, SE, Mann, GE, Sinclair, KD and Webb, R 2008. Nutrition, metabolism, and fertility in dairy cows: 3. Amino acids and ovarian function. Journal of Dairy Science 91, 4190–4197.Google Scholar
Giesy, SL, Yoon, B, Currie, WB, Kim, JW and Boisclair, YR 2012. Adiponectin deficit during the precarious glucose economy of early lactation in dairy cows. Endocrinology 153, 5834–5844.Google Scholar
Gong, JG, Bramley, TA and Webb, R 1993. The effect of recombinant bovine somatotrophin on ovarian follicular growth and development in heifers. Journal of Reproduction and Fertility 97, 247–254.CrossRefGoogle ScholarPubMed
Gulliver, CE, Friend, MA, King, BJ and Clayton, EH 2012. The role of omega-3 polyunsaturated fatty acids in reproduction of sheep and cattle. Animal Reproduction Science 131, 9–22.Google Scholar
Hardie, DG and Carling, D 1997. The AMP-activated protein kinase – fuel gauge of the mammalian cell? European Journal of Biochemistry 246, 259–273.Google Scholar
Harris, SE, Gopichandran, N, Picton, HM, Leese, HJ and Orsi, NM 2005. Nutrient concentrations in murine follicular fluid and the female reproductive tract. Theriogenology 64, 992–1006.Google Scholar
Hawkins, DE, Niswender, KD, Oss, GM, Moeller, CL, Odde, KG, Sawyer, HR and Niswender, GD 1995. An increase in serum lipids increases luteal lipid content and alters the disappearance rate of progesterone in cows. Journal of Animal Science 73, 541–545.Google Scholar
Hemmings, KE, Leese, HJ and Picton, HM 2012. Amino acid turnover by bovine oocytes provides an index of oocyte developmental competence in vitro. Biology of Reproduction 86, 165. 1–12.Google Scholar
Hou, X, Arvisais, EW and Davis, JS 2010. Luteinizing hormone stimulates mammalian target of rapamycin signaling in bovine luteal cells via pathways independent of AKT and mitogen-activated protein kinase: modulation of glycogen synthase kinase 3 and AMP-activated protein kinase. Endocrinology 151, 2846–2857.Google Scholar
Howard, AD, Feighner, SD, Cully, DF, Arena, JP, Liberator, PA, Rosenblum, CI, Hamelin, M, Hreniuk, DL, Palyha, OC, Anderson, J, Paress, PS, Diaz, C, Chou, M, Liu, KK, McKee, KK, Pong, SS, Chaung, LY, Elbrecht, A, Dashkevicz, M, Heavens, R, Rigby, M, Sirinathsinghji, DJ, Dean, DC, Melillo, DG, Patchett, AA, Nargund, R, Griffin, PR, DeMartino, JA, Gupta, SK, Schaeffer, JM, Smith, RG and Van der Ploeg, LH 1996. A receptor in pituitary and hypothalamus that functions in growth hormone release. Science 273, 974–977.Google Scholar
Jia, Z, Zhang, J, Wu, Z and Tian, J 2012. Leptin enhances maturation and development of calf oocytes in vitro. Reproduction in Domestic Animals 47, 718–723.Google Scholar
Jorritsma, R, Cesar, ML, Hermans, JT, Kruitwagen, CL, Vos, PL and Kruip, TA 2004. Effects of non-esterified fatty acids on bovine granulosa cells and developmental potential of oocytes in vitro. Animal Reproduction Science 81, 225–235.Google Scholar
Kadowaki, T and Yamauchi, T 2005. Adiponectin and adiponectin receptors. Endocrine Reviews 26, 439–451.Google Scholar
Kaser, S, Kaser, A, Sandhofer, A, Ebenbichler, CF, Tilg, H and Patsch, JR 2003. Resistin messenger-RNA expression is increased by proinflammatory cytokines in vitro. Biochemical and Biophysical Research Communications 309, 286–290.Google Scholar
Kendall, NR, Gutierrez, CG, Scaramuzzi, RJ, Baird, DT, Webb, R and Campbell, BK 2004. Direct in vivo effects of leptin on ovarian steroidogenesis in sheep. Reproduction 128, 757–765.Google Scholar
Kim, JY, Kinoshita, M, Ohnishi, M and Fukui, Y 2001. Lipid and fatty acid analysis of fresh and frozen-thawed immature and in vitro matured bovine oocytes. Reproduction 122, 131–138.Google Scholar
Kliewer, SA, Sundseth, SS, Jones, SA, Brown, PJ, Wisely, GB, Koble, CS, Devchand, P, Wahli, W, Willson, TM, Lenhard, JM and Lehmann, JM 1997. Fatty acids and eicosanoids regulate gene expression through direct interactions with peroxisome proliferator-activated receptors alpha and gamma. Proceedings of the National Academy of Sciences of the United States of America 94, 4318–4323.Google Scholar
Knickerbocker, JJ, Thatcher, WW, Foster, DB, Wolfenson, D, Bartol, FF and Caton, D 1986. Uterine prostaglandin and blood flow responses to estradiol-17 beta in cyclic cattle. Prostaglandins 31, 757–776.Google Scholar
Kolle, S, Sinowatz, F, Boie, G and Lincoln, D 1998. Developmental changes in the expression of the growth hormone receptor messenger ribonucleic acid and protein in the bovine ovary. Biology of Reproduction 59, 836–842.Google Scholar
Komatsu, T, Itoh, F, Mikawa, S and Hodate, K 2003. Gene expression of resistin in adipose tissue and mammary gland of lactating and non-lactating cows. Journal of Endocrinology 178, R1–R5.CrossRefGoogle ScholarPubMed
Kota, BP, Huang, TH and Roufogalis, BD 2005. An overview on biological mechanisms of PPARs. Pharmacological Research 51, 85–94.Google Scholar
Lagaly, DV, Aad, PY, Grado-Ahuir, JA, Hulsey, LB and Spicer, LJ 2008. Role of adiponectin in regulating ovarian theca and granulosa cell function. Molecular and Cellular Endocrinology 284, 38–45.Google Scholar
Lammoglia, MA, Willard, ST, Oldham, JR and Randel, RD 1996. Effects of dietary fat and season on steroid hormonal profiles before parturition and on hormonal, cholesterol, triglycerides, follicular patterns, and postpartum reproduction in Brahman cows. Journal of Animal Science 74, 2253–2262.Google Scholar
Leroy, JL, Vanholder, T, Delanghe, JR, Opsomer, G, Van Soom, A, Bols, PE and de Kruif, A 2004. Metabolite and ionic composition of follicular fluid from different-sized follicles and their relationship to serum concentrations in dairy cows. Animal Reproduction Science 80, 201–211.Google Scholar
Leroy, JL, Vanholder, T, Mateusen, B, Christophe, A, Opsomer, G, de Kruif, A, Genicot, G and 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.Google Scholar
Lohrke, B, Viergutz, T, Shahi, SK, Pohland, R, Wollenhaupt, K, Goldammer, T, Walzel, H and Kanitz, W 1998. Detection and functional characterisation of the transcription factor peroxisome proliferator-activated receptor gamma in lutein cells. Journal of Endocrinology 159, 429–439.CrossRefGoogle ScholarPubMed
Lorenzo, PL, Illera, MJ, Illera, JC and Illera, M 1994. Enhancement of cumulus expansion and nuclear maturation during bovine oocyte maturation in vitro by the addition of epidermal growth factor and insulin-like growth factor I. Journal of Reproduction and Fertility 101, 697–701.Google Scholar
Lucy, MC 2003. Mechanisms linking nutrition and reproduction in postpartum cows. Reproduction (Cambridge, England) Supplement 61, 415–427.Google Scholar
Lucy, MC, Staples, CR, Michel, FM and Thatcher, WW 1991aEnergy balance and size and number of ovarian follicles detected by ultrasonography in early postpartum dairy cows. Journal of Dairy Science 74, 473–482.Google Scholar
Lucy, MC, Staples, CR, Michel, FM, Thatcher, WW and Bolt, DJ 1991bEffect of feeding calcium soaps to early postpartum dairy cows on plasma prostaglandin F2 alpha, luteinizing hormone, and follicular growth. Journal of Dairy Science 74, 483–489.Google Scholar
Lucy, MC, Curran, TL, Collier, RJ and Cole, WJ 1994. Extended function of the corpus luteum and earlier development of the second follicular wave in heifers treated with bovine somatotropin. Theriogenology 41, 561–572.Google Scholar
Lucy, MC, Bilby, CR, Kirby, CJ, Yuan, W and Boyd, CK 1999. Role of growth hormone in development and maintenance of follicles and corpora lutea. Journal of Reproduction and Fertility Supplement 54, 49–59.Google Scholar
Magalhaes-Padilha, DM, Duarte, AB, Araujo, VR, Saraiva, MV, Almeida, AP, Rodrigues, GQ, Matos, MH, Campello, CC, Silva, JR, Gastal, MO, Gastal, EL and Figueiredo, JR 2012. Steady-state level of insulin-like growth factor-I (IGF-I) receptor mRNA and the effect of IGF-I on the in vitro culture of caprine preantral follicles. Theriogenology 77, 206–213.Google Scholar
Maillard, V, Froment, P, Rame, C, Uzbekova, S, Elis, S and Dupont, J 2011. Expression and effect of resistin on bovine and rat granulosa cell steroidogenesis and proliferation. Reproduction 141, 467–479.Google Scholar
Maillard, V, Uzbekova, S, Guignot, F, Perreau, C, Rame, C, Coyral-Castel, S and Dupont, J 2010. Effect of adiponectin on bovine granulosa cell steroidogenesis, oocyte maturation and embryo development. Reproductive Biology and Endocrinology 8, 23.Google Scholar
Malik, NM, Carter, ND, Murray, JF, Scaramuzzi, RJ, Wilson, CA and Stock, MJ 2001. Leptin requirement for conception, implantation, and gestation in the mouse. Endocrinology 142, 5198–5202.Google Scholar
Mani, AM, Fenwick, MA, Cheng, Z, Sharma, MK, Singh, D and Wathes, DC 2010. IGF1 induces up-regulation of steroidogenic and apoptotic regulatory genes via activation of phosphatidylinositol-dependent kinase/AKT in bovine granulosa cells. Reproduction 139, 139–151.Google Scholar
Marei, WF, Wathes, DC and Fouladi-Nashta, AA 2009. The effect of linolenic Acid on bovine oocyte maturation and development. Biology of Reproduction 81, 1064–1072.Google Scholar
Marei, WF, Wathes, DC and Fouladi-Nashta, AA 2010. Impact of linoleic acid on bovine oocyte maturation and embryo development. Reproduction 139, 979–988.Google Scholar
Marei, WF, Wathes, DC and Fouladi-Nashta, AA 2012. Differential effects of linoleic and alpha-linolenic fatty acids on spatial and temporal mitochondrial distribution and activity in bovine oocytes. Reproduction Fertility and Development 24, 679–690.Google Scholar
Mattos, R, Staples, CR and Thatcher, WW 2000. Effects of dietary fatty acids on reproduction in ruminants. Reviews of Reproduction 5, 38–45.Google Scholar
McEvoy, TG, Coull, GD, Broadbent, PJ, Hutchinson, JS and 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.Google Scholar
Mielenz, M, Mielenz, B, Singh, SP, Kopp, C, Heinz, J, Haussler, S and Sauerwein, H 2013. Development, validation, and pilot application of a semiquantitative Western blot analysis and an ELISA for bovine adiponectin. Domestic Animal Endocrinology 44, 121–130.Google Scholar
Miller, DW, Harrison, JL, Brown, YA, Doyle, U, Lindsay, A, Adam, CL and Lea, RG 2005. Immunohistochemical evidence for an endocrine/paracrine role for ghrelin in the reproductive tissues of sheep. Reproductive Biology and Endocrinology 3, 60.Google Scholar
Mohan, M, Malayer, JR, Geisert, RD and Morgan, GL 2002. Expression patterns of retinoid X receptors, retinaldehyde dehydrogenase, and peroxisome proliferator activated receptor gamma in bovine preattachment embryos. Biology of Reproduction 66, 692–700.Google Scholar
Monget, P, Fabre, S, Mulsant, P, Lecerf, F, Elsen, JM, Mazerbourg, S, Pisselet, C and Monniaux, D 2002. Regulation of ovarian folliculogenesis by IGF and BMP system in domestic animals. Domestic Animal Endocrinology 23, 139–154.CrossRefGoogle ScholarPubMed
Mutinati, M, Desantis, S, Rizzo, A, Zizza, S, Ventriglia, G, Pantaleo, M and Sciorsci, RL 2010. Localization of thyrotropin receptor and thyroglobulin in the bovine corpus luteum. Animal Reproduction Science 118, 1–6.Google Scholar
Nicklin, LT, Robinson, RS, Marsters, P, Campbell, BK, Mann, GE and Hunter, MG 2007. Leptin in the bovine corpus luteum: receptor expression and effects on progesterone production. Molecular Reproduction and Development 74, 724–729.Google Scholar
Nuttinck, F, Charpigny, G, Mermillod, P, Loosfelt, H, Meduri, G, Freret, S, Grimard, B and Heyman, Y 2004. Expression of components of the insulin-like growth factor system and gonadotropin receptors in bovine cumulus-oocyte complexes during oocyte maturation. Domestic Animal Endocrinology 27, 179–195.Google Scholar
Oropeza, A, Wrenzycki, C, Herrmann, D, Hadeler, KG and Niemann, H 2004. Improvement of the developmental capacity of oocytes from prepubertal cattle by intraovarian insulin-like growth factor-I application. Biology of Reproduction 70, 1634–1643.Google Scholar
Paczkowski, M, Silva, E, Schoolcraft, WB and Krisher, RL 2013. Comparative importance of fatty acid beta-oxidation to nuclear maturation, gene expression, and glucose metabolism in mouse, bovine, and porcine cumulus oocyte complexes. Biology of Reproduction 88, 111.Google Scholar
Palin, MF, Bordignon, VV and Murphy, BD 2012. Adiponectin and the control of female reproductive functions. Vitamins & Hormones 90, 239–287.Google Scholar
Patel, L, Buckels, AC, Kinghorn, IJ, Murdock, PR, Holbrook, JD, Plumpton, C, Macphee, CH and Smith, SA 2003. Resistin is expressed in human macrophages and directly regulated by PPAR gamma activators. Biochemical and Biophysical Research Communications 300, 472–476.Google Scholar
Paula-Lopes, FF, Boelhauve, M, Habermann, FA, Sinowatz, F and Wolf, E 2007. Leptin promotes meiotic progression and developmental capacity of bovine oocytes via cumulus cell-independent and -dependent mechanisms. Biology of Reproduction 76, 532–541.Google Scholar
Pehrson, B, Plym Forshell, K and Carlsson, J 1992. The effect of additional feeding on the fertility of high-yielding dairy cows. Zentralbl Veterinarmed A 39, 187–192.Google Scholar
Pikiou, O, Vasilaki, A, Leondaritis, G, Vamvakopoulos, N and Messinis, IE 2013. Effects of metformin on fertilisation of bovine oocytes and early embryo development: possible involvement of AMPK3-mediated TSC2 activation. Zygote 1–10.Google Scholar
Purcell, SH and Moley, KH 2009. Glucose transporters in gametes and preimplantation embryos. Trends in Endocrinology & Metabolism 20, 483–489.CrossRefGoogle ScholarPubMed
Rabiee, AR, Lean, IJ, Gooden, JM and Miller, BG 1999. Relationships among metabolites influencing ovarian function in the dairy cow. Journal of Dairy Science 82, 39–44.Google Scholar
Rabiee, AR, Lean, IJ, Gooden, JM, Miller, BG and Scaramuzzi, RJ 1997. An evaluation of transovarian uptake of metabolites using arterio-venous difference methods in dairy cattle. Animal Reproduction Science 48, 9–25.Google Scholar
Reis, CE, Bressan, J and Alfenas, RC 2010. Effect of the diet components on adiponectin levels. Nutricion Hospitalaria 25, 881–888.Google Scholar
Reverchon, M, Maillard, V, Froment, P, Rame, C and Dupont, J 2013. Adiponectin and resistin: a role in the reproductive functions? Médecine/Sciences (Paris) 29, 417–424.Google Scholar
Rieger, D and Loskutoff, NM 1994. Changes in the metabolism of glucose, pyruvate, glutamine and glycine during maturation of cattle oocytes in vitro. Journal of Reproduction and Fertility 100, 257–262.Google Scholar
Robinson, RS, Pushpakumara, PG, Cheng, Z, Peters, AR, Abayasekara, DR and Wathes, DC 2002. Effects of dietary polyunsaturated fatty acids on ovarian and uterine function in lactating dairy cows. Reproduction 124, 119–131.Google Scholar
Rooke, JA, Ainslie, A, Watt, RG, Alink, FM, McEvoy, TG, Sinclair, KD, Garnsworthy, PC and Webb, R 2009. Dietary carbohydrates and amino acids influence oocyte quality in dairy heifers. Reproduction Fertility and Development 21, 419–427.Google Scholar
Rukkwamsuk, T, Geelen, MJ, Kruip, TA and Wensing, T 2000. Interrelation of fatty acid composition in adipose tissue, serum, and liver of dairy cows during the development of fatty liver postpartum. Journal of Dairy Science 83, 52–59.Google Scholar
Santos, JE, Bilby, TR, Thatcher, WW, Staples, CR and Silvestre, FT 2008. Long chain fatty acids of diet as factors influencing reproduction in cattle. Reproduction in Domestic Animals 43 (suppl. 2), 23–30.Google Scholar
Sarkar, M, Schilffarth, S, Schams, D, Meyer, HH and Berisha, B 2010. The expression of leptin and its receptor during different physiological stages in the bovine ovary. Molecular Reproduction and Development 77, 174–181.Google Scholar
Sato, K, Takahashi, T, Kobayashi, Y, Hagino, A, Roh, SG and Katoh, K 2012. Apelin is involved in postprandial responses and stimulates secretion of arginine-vasopressin, adrenocorticotropic hormone, and growth hormone in the ruminant. Domestic Animal Endocrinology 42, 165–172.CrossRefGoogle ScholarPubMed
Scaramuzzi, RJ, Campbell, BK, Souza, CJ and Baird, DT 2010. Glucose uptake and lactate production by the autotransplanted ovary of the ewe during the luteal and follicular phases of the oestrous cycle. Theriogenology 73, 1061–1067.Google Scholar
Schilffarth, S, Antoni, B, Schams, D, Meyer, HH and Berisha, B 2009. The expression of apelin and its receptor APJ during different physiological stages in the bovine ovary. International Journal of Biological Sciences 5, 344–350.CrossRefGoogle ScholarPubMed
Schwartz, DR and Lazar, MA 2011. Human resistin: found in translation from mouse to man. Trends in Endocrinology & Metabolism 22, 259–265.Google Scholar
Selvaraju, S, Agarwal, SK, Karche, SD, Srivastava, SK, Majumdar, AC and Shanker, U 2002. Fertility responses and hormonal profiles in repeat breeding cows treated with insulin. Animal Reproduction Science 73, 141–149.Google Scholar
Shimizu, T, Kosaka, N, Murayama, C, Tetsuka, M and Miyamoto, A 2009. Apelin and APJ receptor expression in granulosa and theca cells during different stages of follicular development in the bovine ovary: involvement of apoptosis and hormonal regulation. Animal Reproduction Science 116, 28–37.Google Scholar
Shimizu, T, Murayama, C, Sudo, N, Kawashima, C, Tetsuka, M and Miyamoto, A 2008. Involvement of insulin and growth hormone (GH) during follicular development in the bovine ovary. Animal Reproduction Science 106, 143–152.Google Scholar
Shirasuna, K, Shimizu, T, Sayama, K, Asahi, T, Sasaki, M, Berisha, B, Schams, D and Miyamoto, A 2008. Expression and localization of apelin and its receptor APJ in the bovine corpus luteum during the estrous cycle and prostaglandin F2alpha-induced luteolysis. Reproduction 135, 519–525.Google Scholar
Simpson, RB, Chase, CC Jr, Spicer, LJ, Vernon, RK, Hammond, AC and Rae, DO 1994. Effect of exogenous insulin on plasma and follicular insulin-like growth factor I, insulin-like growth factor binding protein activity, follicular oestradiol and progesterone, and follicular growth in superovulated Angus and Brahman cows. Journal of Reproduction and Fertility 102, 483–492.Google Scholar
Sinclair, KD, Sinclair, LA and Robinson, JJ 2000. Nitrogen metabolism and fertility in cattle: I. Adaptive changes in intake and metabolism to diets differing in their rate of energy and nitrogen release in the rumen. Journal of Animal Science 78, 2659–2669.Google Scholar
Spicer, LJ and Echternkamp, SE 1995. The ovarian insulin and insulin-like growth factor system with an emphasis on domestic animals. Domestic Animal Endocrinology 12, 223–245.Google Scholar
Spicer, LJ and Francisco, CC 1997. The adipose obese gene product, leptin: evidence of a direct inhibitory role in ovarian function. Endocrinology 138, 3374–3379.Google Scholar
Spicer, LJ and Francisco, CC 1998. Adipose obese gene product, leptin, inhibits bovine ovarian thecal cell steroidogenesis. Biology of Reproduction 58, 207–212.Google Scholar
Spicer, LJ, Alpizar, E and Vernon, RK 1994. Insulin-like growth factor-I receptors in ovarian granulosa cells: effect of follicle size and hormones. Molecular and Cellular Endocrinology 102, 69–76.Google Scholar
Spicer, LJ, Chamberlain, CS and Francisco, CC 2000. Ovarian action of leptin: effects on insulin-like growth factor-I-stimulated function of granulosa and thecal cells. Endocrine 12, 53–59.Google Scholar
Spicer, LJ, Alonso, J and Chamberlain, CS 2001. Effects of thyroid hormones on bovine granulosa and thecal cell function in vitro: dependence on insulin and gonadotropins. Journal of Dairy Science 84, 1069–1076.Google Scholar
Spicer, LJ, Schreiber, NB, Lagaly, DV, Aad, PY, Douthit, LB and Grado-Ahuir, JA 2011. Effect of resistin on granulosa and theca cell function in cattle. Animal Reproduction Science 124, 19–27.Google Scholar
Staples, CR, Burke, JM and Thatcher, WW 1998. Influence of supplemental fats on reproductive tissues and performance of lactating cows. Journal of Dairy Science 81, 856–871.Google Scholar
Stefanello, JR, Barreta, MH, Porciuncula, PM, Arruda, JN, Oliveira, JF, Oliveira, MA and Goncalves, PB 2006. Effect of angiotensin II with follicle cells and insulin-like growth factor-I or insulin on bovine oocyte maturation and embryo development. Theriogenology 66, 2068–2076.Google Scholar
Sturmey, RG, Reis, A, Leese, HJ and 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.Google Scholar
Sundvold, H, Brzozowska, A and Lien, S 1997. Characterisation of bovine peroxisome proliferator-activated receptors gamma 1 and gamma 2: genetic mapping and differential expression of the two isoforms. Biochemical and Biophysical Research Communications 239, 857–861.Google Scholar
Sutton-McDowall, ML, Gilchrist, RB and Thompson, JG 2010. The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 139, 685–695.Google Scholar
Tabandeh, MR, Hosseini, A, Saeb, M, Kafi, M and Saeb, S 2010. Changes in the gene expression of adiponectin and adiponectin receptors (AdipoR1 and AdipoR2) in ovarian follicular cells of dairy cow at different stages of development. Theriogenology 73, 659–669.Google Scholar
Tabandeh, MR, Golestani, N, Kafi, M, Hosseini, A, Saeb, M and Sarkoohi, P 2012. Gene expression pattern of adiponectin and adiponectin receptors in dominant and atretic follicles and oocytes screened based on brilliant cresyl blue staining. Animal Reproduction Science 131, 30–40.Google Scholar
Tatemoto, K, Hosoya, M, Habata, Y, Fujii, R, Kakegawa, T, Zou, MX, Kawamata, Y, Fukusumi, S, Hinuma, S, Kitada, C, Kurokawa, T, Onda, H and Fujino, M 1998. Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochemical and Biophysical Research Communications 251, 471–476.Google Scholar
Tersigni, C, Di Nicuolo, F, D’Ippolito, S, Veglia, M, Castellucci, M and Di Simone, N 2011. Adipokines: new emerging roles in fertility and reproduction. Obstetrical and Gynecological Survey 66, 47–63.Google Scholar
Thatcher, W, Santos, JE and Staples, CR 2011. Dietary manipulations to improve embryonic survival in cattle. Theriogenology 76, 1619–1631.Google Scholar
Thomas, FH, Campbell, BK, Armstrong, DG and Telfer, EE 2007. Effects of IGF-I bioavailability on bovine preantral follicular development in vitro. Reproduction 133, 1121–1128.Google Scholar
Tontonoz, P, Hu, E and Spiegelman, BM 1995. Regulation of adipocyte gene expression and differentiation by peroxisome proliferator activated receptor gamma. Current Opinion in Genetics & Development 5, 571–576.CrossRefGoogle ScholarPubMed
Tosca, L, Chabrolle, C and Dupont, J 2008. AMPK: a link between metabolism and reproduction? Médecine/Sciences (Paris) 24, 297–300.Google Scholar
Tosca, L, Chabrolle, C, Uzbekova, S and Dupont, J 2007aEffects of metformin on bovine granulosa cells steroidogenesis: possible involvement of adenosine 5' monophosphate-activated protein kinase (AMPK). Biology of Reproduction 76, 368–378.Google Scholar
Tosca, L, Uzbekova, S, Chabrolle, C and Dupont, J 2007bPossible role of 5'AMP-activated protein kinase in the metformin-mediated arrest of bovine oocytes at the germinal vesicle stage during in vitro maturation. Biology of Reproduction 77, 452–465.Google Scholar
Tosca, L, Rame, C, Chabrolle, C, Tesseraud, S and Dupont, J 2010. Metformin decreases IGF1-induced cell proliferation and protein synthesis through AMP-activated protein kinase in cultured bovine granulosa cells. Reproduction 139, 409–418.Google Scholar
Van Hoeck, V, Sturmey, RG, Bermejo-Alvarez, P, Rizos, D, Gutierrez-Adan, A, Leese, HJ, Bols, PE and Leroy, JL 2011. Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology. PLoS One 6, e23183.Google Scholar
Van Hoeck, V, Leroy, JL, Arias Alvarez, M, Rizos, D, Gutierrez-Adan, A, Schnorbusch, K, Bols, PE, Leese, HJ and Sturmey, RG 2013. Oocyte developmental failure in response to elevated nonesterified fatty acid concentrations: mechanistic insights. Reproduction 145, 33–44.Google Scholar
Vanholder, T, Leroy, JL, Soom, AV, Opsomer, G, Maes, D, Coryn, M de Kruif, A 2005. Effect of non-esterified fatty acids on bovine granulosa cell steroidogenesis and proliferation in vitro. Animal Reproduction Science 87, 33–44.Google Scholar
van Tol, HT, van Eerdenburg, FJ, Colenbrander, B and Roelen, BA 2008. Enhancement of Bovine oocyte maturation by leptin is accompanied by an upregulation in mRNA expression of leptin receptor isoforms in cumulus cells. Molecular Reproduction and Development 75, 578–587.Google Scholar
Velazquez, MA, Hadeler, KG, Herrmann, D, Kues, WA, Remy, B, Beckers, JF and Niemann, H 2012. In vivo oocyte IGF-1 priming increases inner cell mass proliferation of in vitro-formed bovine blastocysts. Theriogenology 78, 517–527.Google Scholar
Vidal-Puig, A, Jimenez-Linan, M, Lowell, BB, Hamann, A, Hu, E, Spiegelman, B, Flier, JS and Moller, DE 1996. Regulation of PPAR gamma gene expression by nutrition and obesity in rodents. Journal of Clinical Investigation 97, 2553–2561.Google Scholar
Viergutz, T, Loehrke, B, Poehland, R, Becker, F and Kanitz, W 2000. Relationship between different stages of the corpus luteum and the expression of the peroxisome proliferator-activated receptor gamma protein in bovine large lutein cells. Journal of Reproduction and Fertility 118, 153–161.Google Scholar
Wade, GN and Schneider, JE 1992. Metabolic fuels and reproduction in female mammals. Neuroscience & Biobehavioral Reviews 16, 235–272.Google Scholar
Waku, T, Shiraki, T, Oyama, T, Fujimoto, Y, Maebara, K, Kamiya, N, Jingami, H and Morikawa, K 2009. Structural insight into PPARgamma activation through covalent modification with endogenous fatty acids. Journal of Molecular Biology 385, 188–199.Google Scholar
Wang, Q, Chi, MM, Schedl, T and Moley, KH 2012. An intercellular pathway for glucose transport into mouse oocytes. American Journal of Physiology: Endocrinology and Metabolism 302, E1511–E1518.Google Scholar
Wang, Z, Lin, P and Yu, S 2013. Effects of ghrelin on developmental competence and gene expression of in vitro fertilized ovine embryos. Theriogenology 79, 695–701.Google Scholar
Wathes, DC, Abayasekara, DR and Aitken, RJ 2007. Polyunsaturated fatty acids in male and female reproduction. Biology of Reproduction 77, 190–201.Google Scholar
Watson, AJ, De Sousa, P, Caveney, A, Barcroft, LC, Natale, D, Urquhart, J and Westhusin, ME 2000. Impact of bovine oocyte maturation media on oocyte transcript levels, blastocyst development, cell number, and apoptosis. Biology of Reproduction 62, 355–364.Google Scholar
Webb, R, Garnsworthy, PC, Gong, JG and Armstrong, DG 2004. Control of follicular growth: local interactions and nutritional influences. Journal of Animal Science 82 (E-suppl.), E63–E74.Google Scholar
Wehrman, ME, Welsh, TH Jr and Williams, GL 1991. Diet-induced hyperlipidemia in cattle modifies the intrafollicular cholesterol environment, modulates ovarian follicular dynamics, and hastens the onset of postpartum luteal activity. Biology of Reproduction 45, 514–522.Google Scholar
Zeron, Y, Sklan, D and Arav, A 2002. Effect of polyunsaturated fatty acid supplementation on biophysical parameters and chilling sensitivity of ewe oocytes. Molecular Reproduction and Development 61, 271–278.Google Scholar
Zhang, SS, Carrillo, AJ and Darling, DS 1997. Expression of multiple thyroid hormone receptor mRNAs in human oocytes, cumulus cells, and granulosa cells. Molecular Human Reproduction 3, 555–562.Google Scholar
Zuelke, KA and Brackett, BG 1993. Increased glutamine metabolism in bovine cumulus cell-enclosed and denuded oocytes after in vitro maturation with luteinizing hormone. Biology of Reproduction 48, 815–820.Google Scholar