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Elevated free fatty acids affect bovine granulosa cell function: a molecular cue for compromised reproduction during negative energy balance.

ABSTRACT: High-yielding dairy cows postpartum face the challenge of negative energy balance leading to elevated free fatty acids levels in the serum and follicular fluid thus affecting the ovarian function. Here, we investigated effects of physiological concentrations of palmitic acid (PA), stearic acid (SA) and oleic acid (OA) on the viability, steroid production and gene expression in a bovine granulosa cell (GC) culture model. Treatment with individual and combined fatty acids increased the CD36 gene expression, while no significant apoptotic effects were observed. Both PA and SA significantly upregulated the expression of FSHR, LHCGR, CYP19A1, HSD3B1, CCND2 and increased 17?-estradiol (E2) production, while OA downregulated the expression of these genes and reduced E2. Interestingly, STAR was equally downregulated by all fatty acids and combination treatment. E2 was significantly reduced after combination treatment. To validate the effects of OA, in vivo growing dominant follicles (10-19 mm) were injected with bovine serum albumin (BSA) with/without conjugated OA. The follicular fluid was recovered 48 h post injection. As in our in vitro model, OA significantly reduced intrafollicular E2 concentrations. In addition, expression of CD36 was significantly up- and that of CYP19A1 and STAR significantly downregulated in antral GC recovered from aspirated follicles. The ovulation rates of OA-injected follicles tended to be reduced. Our results indicate that elevated free fatty acid concentrations specifically target functional key genes in GC both in vitro and in vivo. Suggestively, this could be a possible mechanism through which elevated free fatty acids affect folliculogenesis in dairy cows postpartum.

SUBMITTER: Sharma A

PROVIDER: S-EPMC6479201 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Elevated free fatty acids affect bovine granulosa cell function: a molecular cue for compromised reproduction during negative energy balance.

Sharma Arpna A Baddela Vijay Simha VS Becker Frank F Dannenberger Dirk D Viergutz Torsten T Vanselow Jens J

Endocrine connections 20190501 5

High-yielding dairy cows postpartum face the challenge of negative energy balance leading to elevated free fatty acids levels in the serum and follicular fluid thus affecting the ovarian function. Here, we investigated effects of physiological concentrations of palmitic acid (PA), stearic acid (SA) and oleic acid (OA) on the viability, steroid production and gene expression in a bovine granulosa cell (GC) culture model. Treatment with individual and combined fatty acids increased the CD36 gene e ...[more]

PMID: 30925464

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Project description:ABSTRACT:Oxidative stress and telomere dynamics are considered to be powerful biomarkers quantifying a potential trade-off between current reproduction and self-maintenance. Recent studies confirmed the negative impact of elevated reproduction on telomeres, but the evidence for the cost of reproduction in terms of oxidative stress remains equivocal. In order to induce reproductive costs, we experimentally manipulated reproductive effort by increasing brood size in captive zebra finches (Taeniopygia guttata) and additionally challenged all birds by a low ambient temperature to facilitate detection of these costs. We were not able to show any negative effects of elevated reproductive effort on telomere dynamics and oxidative stress among parents, although brood enlargement was effective in terms of total mass and number of fledged young. Interestingly, irrespective of brood size treatment, we found a significant increase in antioxidant capacity at peak breeding while oxidative damage did not change with time. Our results may suggest that reproduction, instead of generating costs, may stimulate physiological functions promoting self-maintenance in terms of higher protection against free radicals. Possibly, opportunistic breeders such as zebra finches may not impede their future performance for the sake of current reproduction. SIGNIFICANCE STATEMENT:This study interrogates a molecular background behind one of the most intriguing trade-offs that potentially occurs between self-maintenance and reproduction. We manipulated breeding effort in zebra finches to understand if the cost of reproduction can be mediated by telomere dynamics and oxidative stress. In our study system, we did not detect the direct reproductive costs in terms of parental oxidative damage and telomere loss; instead, these costs were paid by the offspring in terms of their inhibited growth rate. Moreover, we found that entering into the reproductive state strongly stimulated self-maintenance by increasing antioxidant capacity in parents. Our results emphasize that current reproductive success is not always prioritized over investment in body maintenance preventing the oxidative cost of reproduction.

Project description:Our objectives were to compare gene expression profiles in neutrophils (PMN) during a Streptococcus uberis mastitis challenge between lactating cows subjected to feed restriction to induce negative energy balance (NEB; n = 5) and cows fed ad libitum to maintain positive energy balance (PEB; n = 5). The NEB cows were feed-restricted to 60% of calculated net energy for lactation requirements for 7 d, whereas PEB cows were fed the same diet for ad libitum intake. After 5 d of feed restriction, one rear mammary quarter of each cow was inoculated with 5,000 cfu of Streptococcus uberis (strain O140J). Blood PMN were isolated at 24 h post-inoculation from all cows for RNA extraction and microarray analysis. NEB resulted in 94 differentially expressed genes compared with PEB. Of these, 51 genes were down-regulated, including genes involved with antigen presentation (HLADRA and HLAA), respiratory burst (SOD1), and the pro-inflammatory response (TNFA and IRAK-1). The most affected genes up-regulated by NEB (n = 43) included IL1R2 and IL6, toll-like receptors (TLR2 and TLR4), and THY1. Network analysis by Ingenuity Pathway Analysis Â® revealed that TNFA was associated with the expression of numerous differentially expressed genes involved with immune response in NEB cows compared with PEB cows. Energy balance alters PMN expression of several genes involved with immune response, which provides new information on transcriptomic mechanisms associated with post-partal NEB and immune response during early lactation. Briefly, 10 multiparous Holstein cows in PEB and past peak lactation were used for this study. The NEB cows were feed-restricted to 60% of calculated NEL requirements for 7 d, whereas PEB cows were fed the same diet for ad libitum intake. After 5 d of feed restriction, one rear mammary quarter of each cow was inoculated with 5,000 cfu of Streptococcus uberis (strain O140J). Blood PMN were isolated at 24 h post-inoculation from all cows. A 13,257-oligonucleotide (70-mers) array was used for transcript profiling. Cy3- and Cy5 labelled cDNA from PMN and a reference standard were used for hybridizations. All samples were hybridized to duplicate slides with reverse labeling (20 microarrays total).

Dataset Information

Elevated free fatty acids affect bovine granulosa cell function: a molecular cue for compromised reproduction during negative energy balance.

Publications

Elevated free fatty acids affect bovine granulosa cell function: a molecular cue for compromised reproduction during negative energy balance.

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