Negative energy balance affects imprint stability in oocytes recovered from postpartum dairy cows

Abstract

Ovarian follicle development in post-partum, high-producing dairy cows, occurs in a compromised endogenous metabolic environment (referred to as negative energy balance, NEB). Key events that occur during oocyte/follicle growth, such as the vital process of genomic imprinting, may be detrimentally affected by this altered ovarian environment. Imprinting is crucial for placental function and regulation of fetal growth, therefore failure to establish and maintain imprints during oocyte growth may contribute to early embryonic loss. Using ovum pick-up (OPU), oocytes and follicular fluid samples were recovered from cows between days 20 and 115 post-calving, encompassing the NEB period. In a complimentary study, cumulus oocyte complexes were in vitro matured under high non-esterified fatty acid (NEFA) concentrations and in the presence of the methyl-donor S-adenosylmethionine (SAM). Pyrosequencing revealed the loss of methylation at several imprinted loci in the OPU derived oocytes. The loss of DNA methylation was observed at the PLAGL1 locus in oocytes, following in vitro maturation (IVM) in the presence of elevated NEFAs and SAM. Finally, metabolomic analysis of postpartum follicular fluid samples revealed significant differences in several branched chain amino acids, with fatty acid profiles bearing similarities to those characteristic of lactating dairy cows. These results provide the first evidence that (1) the postpartum ovarian environment may affect maternal imprint acquisition and (2) elevated NEFAs during IVM can lead to the loss of imprinted gene methylation in bovine oocytes.

Exposure of bovine oocytes and embryos to elevated non-esterified fatty acid concentrations: integration of epigenetic and transcriptomic signatures in resultant blastocysts

“…Using a bovine model, we and others have previously shown that elevated NEFA concentrations during oocyte maturation and embryo culture are detrimental for embryonic development [1, 3]. Additionally, elevated NEFA levels in the oocyte’s microenvironment can affect gene expression, DNA methylation at imprinted genes and alter the phenotype of resultant blastocysts [4–6]. Lower cell numbers and increased apoptosis were observed in blastocysts after exposure of oocytes to elevated NEFA concentrations.…”

Extent of adaptation of high yielding murrah buffaloes to negative energy balance in response to various dry period lengths

“…Improved energy status in short dry period group will fasten the postpartum ovulation, thus decreasing the service period and increasing reproductive efficiency (De Feu et al 2009). In addition, the total number of services required for conception was more with less insemination success rate in group I, compared to the other two groups indicating reduced quality of oocytes (O'Doherty et al, 2014). dry period (60 or > 60 days).…”

“…Further, it has been well documented that the severity and duration of NEB are positively associated with the interval to first postpartum ovulation. In addition, NEB exerts negative effects on the imprint stability in the oocytes, reducing conception rates during first weeks of the breeding season (O'Doherty et al, 2014). So, a study has been carried out to evaluate the extent of adaptation of high yielding buffaloes to negative energy balance in response to various dry period lengths, by using serum NEFA, ANEFAP levels and days required for postpartum conception as indicators.…”

Invited review: Reproductive and genomic technologies to optimize breeding strategies for genetic progress in dairy cattle

“…Grossniklaus et al, 2013;Heard and Martienssen, 2014;Blake and Watson, 2016). Despite the limited number of epigenetic studies in dairy cattle, they have covered milk production (Singh et al, 2010), reproduction (Sun et al, 2013;Walker et al, 2013;Saadi et al, 2017;O'Doherty et al, 2014), ageing (Green et al, 2015), and health (e.g. Green and Kerr, 2014;Doherty et al, 2016).…”