Elevated Non-Esterified Fatty Acid Concentrations during Bovine Oocyte Maturation Compromise Early Embryo Physiology

Hoeck, Veerle Van; Sturmey, Roger G.; Bermejo-Álvarez, Pablo; Rizos, Dimitrios; Gutiérrez‐Adán, Alfonso; Leese, Henry J.; Bols, P.E.J.; Leroy, Jo

doi:10.1371/journal.pone.0023183

Cited by 240 publications

(190 citation statements)

References 63 publications

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“…Perhaps the best-studied example of a metabolic imprint is for postpartum NEFA and its effect on composition of the oocyte and function of follicular cells Van Hoeck et al, 2011;Wathes, 2012). The possibility that there are permanent epigenetic modifications to the genome during the early postpartum period that affect long-term developmental competence of follicular cells has not been demonstrated at this time.…”

Section: Lucy Butler and Garverickmentioning

confidence: 99%

Endocrine and metabolic mechanisms linking postpartum glucose with early embryonic and foetal development in dairy cows

Lucy

Butler

Garverick

2014

Animal

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Milk and milk solids production per cow is increasing annually in dairy systems. Peak milk production is in early lactation when the uterus and ovary are recovering from the previous pregnancy. The competing processes of milk production and restoration of reproductive function can be at odds, particularly if unique homeorhetic mechanisms that typify early lactation become imbalanced and cows experience metabolic disease. Homeorhesis leads to an increase in the synthesis of glucose that is irreversibly lost to milk lactose. Irreversible loss of glucose during lactation can invoke an endocrine and metabolic state that impinges upon postpartum uterine health, oestrous cyclicity and subsequent establishment of pregnancy. The first 30 days postpartum may be most critical in terms of the impact that metabolites and metabolic hormones have on reproduction. Depressed immune function caused in part by the postpartum metabolic profile leads to a failure in uterine involution and uterine disease. Oestrous cyclicity (interval to first ovulation and subsequent periodicity) is affected by the same hormones and metabolites that control postpartum immune function. Slower growth of the embryo or foetus perhaps explained by the unique metabolic profile during lactation may predispose cows to pregnancy loss. Understanding homeorhetic mechanisms that involve glucose and collectively affect postpartum uterine health, oestrous cyclicity and the establishment of pregnancy should lead to methods to improve postpartum fertility in dairy cows.Keywords: glucose, IGF1, insulin, pregnancy, dairy cow ImplicationsCompeting processes of milk production and reproduction can be at odds in dairy cows, particularly if the unique metabolic processes that typify early lactation become imbalanced. A potential end result is that cows do not become pregnant during the breeding period. The need to replace infertile cows adds to the cost of production. Understanding basic mechanisms that link the first 60 days of lactation with the subsequent success or failure of establishing pregnancy during the breeding period, therefore, is an important area of research for the dairy industry. IntroductionWithin most dairy production systems, milk or milk solids production per cow is increasing annually. The average United States dairy cow, for example, produces in excess of 9500 kg of milk annually. Peak milk production is in early lactation (within 30 to 60 days after calving) when the uterus is involuting and the ovary is restoring the cyclic processes that lead to oestrus, ovulation, and the formation of a corpus luteum. Competing processes of milk production, uterine involution, and the restoration of ovarian activity can be at odds, particularly if the unique homeorhetic processes that typify early lactation become imbalanced and there is metabolic disease. A potential end result of the competition between high milk production and the reproductive system is that cows do not become pregnant during the breeding period which is typically initiated at~60 days after...

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Section: Lucy Butler and Garverickmentioning

confidence: 99%

Endocrine and metabolic mechanisms linking postpartum glucose with early embryonic and foetal development in dairy cows

Lucy

Butler

Garverick

2014

Animal

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“…The marked differences between cows and heifers justify further comparison of their calves. Previous work has demonstrated that the factor 'lactation' alters embryo quality compared with non-lactating cows (Leroy et al, 2005), and that exposure of bovine oocytes to NEB conditions in vitro affects glucose homeostasis in early embryonic stages (Van Hoeck et al, 2011 and. The difference in IGF-I corresponds to other reports (Taylor et al, 2004) and is of particular interest, since IGF-I has been proposed as a mediator between maternal energy balance and foetal development (Wathes et al, 1998;Lucy, 2008;Micke et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

Effects of parity and periconceptional metabolic state of Holstein–Friesian dams on the glucose metabolism and conformation in their newborn calves

Bossaert

Fransén

Langbeen

et al. 2014

Animal

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The metabolic state of pregnant mammals influences the offspring's development and risk of metabolic disease in postnatal life. The metabolic state in a lactating dairy cow differs immensely from that in a non-lactating heifer around the time of conception, but consequences for their calves are poorly understood. The hypothesis of this study was that differences in metabolic state between non-lactating heifers and lactating cows during early pregnancy would affect insulin-dependent glucose metabolism and development in their neonatal calves. Using a mixed linear model, concentrations of glucose, IGF-I and non-esterified fatty acids (NEFAs) were compared between 13 non-lactating heifers and 16 high-yielding dairy cows in repeated blood samples obtained during the 1st month after successful insemination. Calves born from these dams were weighed and measured at birth, and subjected to intravenous glucose and insulin challenges between 7 and 14 days of age. Eight estimators of insulin-dependent glucose metabolism were determined: glucose and insulin peak concentration, area under the curve and elimination rate after glucose challenge, glucose reduction rate after insulin challenge, and quantitative insulin sensitivity check index. Effects of dam parity and calf sex on the metabolic and developmental traits were analysed in a two-way ANOVA. Compared with heifers, cows displayed lower glucose and IGF-I and higher NEFA concentrations during the 1st month after conception. However, these differences did not affect developmental traits and glucose homeostasis in their calves: birth weight, withers height, heart girth, and responses to glucose and insulin challenges in the calves were unaffected by their dam's parity. In conclusion, differences in the metabolic state of heifers and cows during early gestation under field conditions could not be related to their offspring's development and glucose homeostasis.

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“…A recent study has shown that exposure of the maturing oocytes to elevated concentrations of NEFAs has a negative impact on fertility not only through a reduction in the developmental capacity of the oocyte but also through compromised quality, viability and metabolic capacity of the early embryos (Van Hoeck et al, 2011). The same laboratory suggests that these negative effects of NEFAs on the embryo could be a consequence of modified energy metabolism and particularly, mitochondrial β-oxidation of fatty acids in the oocyte (Van Hoeck et al, 2013). A recent study has shown that bovine cumulus cells are able to protect maturing oocytes from potential harmful effects of increased local concentrations of fatty acids by intracellular storage of lipids (Aardema et al, 2013).…”

Section: Nefasmentioning

confidence: 99%

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

Dupont

Scaramuzzi

Reverchon

2014

animal

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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.

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Elevated Non-Esterified Fatty Acid Concentrations during Bovine Oocyte Maturation Compromise Early Embryo Physiology

Cited by 240 publications

References 63 publications

Endocrine and metabolic mechanisms linking postpartum glucose with early embryonic and foetal development in dairy cows

Endocrine and metabolic mechanisms linking postpartum glucose with early embryonic and foetal development in dairy cows

Effects of parity and periconceptional metabolic state of Holstein–Friesian dams on the glucose metabolism and conformation in their newborn calves

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

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