Abstract
Simple SummaryThe placenta plays an important role in the growth and development of a fetus and in maintaining a healthy pregnancy. The placenta is also sensitive to suboptimal intrauterine conditions, such as maternal obesity. Although previous studies have indicated that maternal obesity is associated with placental dysfunction, we are still far from elucidating the molecular mechanisms underlying this phenomenon. In this study, proteomic technique was employed to compare the proteomic profiles of the placentas of sows with different backfat thicknesses. We revealed that excessive backfat of sow is associated with abnormal carbohydrate and lipid metabolism, mitochondrial dysfunction, and increased oxidative stress and inflammation in the placenta. Our results promote the understanding of decreased placental efficiency induced by maternal obesity.Maternal obesity is associated with impaired maternal metabolism and affects the developmental programming of the fetus. The placenta is dysfunctional when exposed to an obese intrauterine environment and can transduce and mediate detrimental maternal impacts to the fetus through mechanisms that remain largely unknown. The main objective of this study was to investigate the effects of maternal obesity on the porcine placental proteome and to analyze the deregulated proteins and potential pathways predicted to be disturbed in obese placentas, using sows with high backfat as a model of obese pregnancy. The sows were divided into two groups based on their backfat thickness: normal backfat (NBF, 17–22 mm; n = 30) and high backfat (HBF, ≥23 mm; n = 30) as the maternal obesity group. The placental tissues used for the proteomic and biochemical analyses were obtained through vaginal delivery, and the maternal blood samples used to determine the metabolic parameters were collected at day 107 of pregnancy. Our study demonstrated that HBF sows had significantly decreased placental efficiency, increased plasma-free fatty acids and triglyceride levels, and increased proinflammatory cytokines plasma levels (p < 0.05). HBF placentas had significantly higher malondialdehyde level, lower total antioxidant capacity and antioxidase activity, increased triglyceride content and enhanced proinflammatory tumor necrosis factor- α (TNF-α) and interleukin-6 (IL-6) contents (p < 0.05). Among the 4652 proteins identified using the proteomic method, 343 were quantified as differentially abundant proteins, which were involved in many vital biological processes. Based on our bioinformatic and placental biochemical analyses, we concluded that maternal obesity is associated with abnormal carbohydrate and lipid metabolism, mitochondrial dysfunction, decreased steroid hormone biosynthesis, and increased oxidative stress and inflammation in the placenta. The results of this study are undoubtedly valuable to other researchers.
Highlights
The prevalence of maternal obesity has increased dramatically [1] and is associated with impaired fecundity in humans as well as in some animals, such as pigs [2,3]
The number of low body weight piglets (LBW, piglets with weight < 0.9 kg), percentage of stillborn piglets and within-litter variation of piglet weights were significantly greater in the high backfat (HBF) sows
We observed that HBF placentas had significantly increased TG content
Summary
The prevalence of maternal obesity has increased dramatically [1] and is associated with impaired fecundity in humans as well as in some animals, such as pigs [2,3]. Recent evidences demonstrate that maternal obesity results in lipotoxicity characterized by ectopic fat accumulation [8], augmented inflammatory responses and macrophage accumulation [9], and elevated nitrative and oxidative stress [10,11] in the human placenta, which may promote impaired trophoblast functions and alterations in placental nutrient transport [12]. The challenge of intrauterine stress associated with maternal obesity is that it can disrupt normal placental function, and impact fetal growth and development through mechanisms that remain largely unknown
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