Role of Fatty Acids in Energy Provision During Oocyte Maturation and Early Embryo Development

Abstract

While much is known about the metabolism of exogenous nutrients such as glucose, lactate, pyruvate, amino acids by oocytes and pre-implantation mammalian embryos, the role of endogenous stores, particularly lipid, has been largely overlooked. The presence of lipid within oocytes and early embryos has been long known, and comparisons between species indicate that the amounts and types of lipid present vary considerably. Large amounts of intracellular lipid can compromise the success of cryopreservation and the removal of such lipid has been the subject of considerable effort. In this review, we present evidence that strongly suggests a metabolic role for lipid, specifically with regard to energy provision, in the late-stage oocyte and the pre-implantation embryo. We focus initially on oxygen consumption as a global indicator of metabolic activity, before reviewing different approaches that either have been designed to investigate directly, or have revealed indirectly the role of endogenous lipid in energy generation. These fall under five headings: (i) fatty acid oxidation; (ii) inhibition of triglyceride oxidation; (iii) culture in the absence of exogenous substrates; (iv) cytoplasmic organization; and (v) delipidation. On the basis of the data derived from these studies, we conclude that there is strong evidence for the utilization of endogenous lipid as an energy substrate by oocytes and early embryos.

Effect of Linolenic acid during in vitro maturation of ovine oocytes: embryonic developmental potential and mRNA abundances of genes involved in apoptosis

“…Although numerous studies have advanced knowledge of the influence of fat and mix of fatty acids on oocyte developmental competence [9][10][11][12][13], data on the effect of each family or each specific fatty acid are rare and the results of the existing studies are somewhat discordant. All-cis-9,12,15-octadecatrienoic acid or α-linolenic acid (ALA,18:3 n-3, an essential fatty acid of the ω-3 family) is a PUFA highly abundant in some vegetable oils and sea fishes [14].…”

Impact of contrasting fish oil concentrations in the diet on ovine embryo development <i>in vivo</i> and of corresponding diet-specific derivative sera during <i>in vitro</i> culture

“…Yet, on the basis of their ability to alter the expression of the uterine IGF system in a way that is conducive to good embryo survival, the PUFAs of fish oil are regarded as having the potential for improving the reproductive performance of the high-yielding dairy cow (Coyne et al, 2011). This dichotomy, whereby potentially beneficial lipid-derived stimuli for endocrine functions or prostaglandin attenuation are co-incident with a capacity for direct and detrimental effects on oocyte/embryo competence (Kuran et al, 1999;McEvoy et al, 2000a;Robinson et al, 2002b;Leroy et al, 2008;Sturmey et al, 2009), reinforces the argument that both careful dietary management and further study of various lipid-linked effects in vivo and in vitro are warranted. In cattle and sheep oocytes, polyunsaturated fatty acids constitute only a minor proportion of acyl-containing lipids; and among them both EPA and DHA are found in modest amounts, together comprising less than 5% (w/w) of total fatty acids in oocyte lipid (McEvoy et al, 2000b); these are nevertheless two developmentally-significant long-chain PUFAs, of which fish oil is a rich source.…”

“…Fatty acid inclusion in embryo culture systems is not new (Kane, 1979) but much remains to be discovered about these compounds which as well as being sources of energy (Sturmey et al, 2009) have, along with their derivatives, numerous biological roles mediated on the basis of both structure and function, most critically perhaps via their influences on membrane composition, fluidity and resilience. Here the addition to the embryo culture medium of serum harvested from ewes receiving the fish oil supplements at the 3% dietary inclusion rate had no adverse effects on the number and diameter of day 6 and 7 blastocysts compared with serum from control ewes and indeed slightly improved the proportion of blastocysts of very good quality (Grades 1 to 1.5).…”

“…In the context of the present investigations on fatty acids, the literature on their role as energy providers for the oocyte and early embryo points to their use from both endogenous and exogenous sources (Sturmey et al, 2009). Dietary lipid supplements have been shown in numerous studies to improve dairy cow fertility either through the correction of an essential fatty acid deficiency or via an enhancement of the endocrine and immune systems.…”

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

“…Compared with rodents, the oocytes and embryos of farm animals including cattle contain relatively high levels of intracellular lipids, with triglycerides being the major component. For example, the mouse oocyte contains 4 ng of triglyceride, whereas the cow oocyte contains 63 ng, and the sheep oocyte contains 89 ng (McEvoy et al, 2000;Sturmey et al, 2009). Fatty acids are an endogenous source of energy during oocyte maturation; several lines of evidence support the idea of fatty-acid oxidation as a source of essential ATP for oocyte maturation and for early development of the embryo.…”