Maternal dietary antioxidant supplementation regulates weaned piglets' adipose tissue transcriptome and morphology

PLoS One. 2024 Sep 12;19(9):e0310399. doi: 10.1371/journal.pone.0310399. eCollection 2024.

Abstract

Antioxidant supplementation in critical periods may be useful for improvement of piglet early viability and development. We have evaluated the effects of maternal perinatal diet inclusion of a high vitamin E level (VE, 100 mg all-rac-α-tocopheryl acetate /kg), hydroxytyrosol (HT, 1.5 mg/kg), or their combination (VEHT), in comparison to a control diet (C, 30 mg all-rac-α-tocopheryl acetate /kg), on the offspring homeostasis and metabolism, analysing the weaned piglets' adipose tissue transcriptome and adipocyte morphology. Diets were provided to pregnant Iberian sows (n = 48, 12 per treatment) from gestation day 85 to weaning (28 days postpartum) and 48 piglets (n = 12 per treatment) were sampled 5 days postweaning for dorsal subcutaneous adipose tissue analyses. RNA obtained from 6 animals for each diet was used for paired-end RNA sequencing. Results show that supplementation of sows' diet with either vitamin E or hydroxytyrosol had substantial effects on weaned piglet adipose transcriptome, with 664 and 587 genes being differentially expressed, in comparison to C, respectively (q-value<0.10, Fold Change>1.5). Genes upregulated in C were mainly involved in inflammatory and immune response, as well as oxidative stress, and relevant canonical pathways and upstream regulators involved in these processes were predicted as activated, such as TNF, IFNB or NFKB. Vitamin E, when supplemented alone at high dose, activated lipid biosynthesis functions, pathways and regulators, this finding being accompanied by increased adipocyte size. Results suggest an improved metabolic and antioxidant status of adipose tissue in animals born from sows supplemented with individual antioxidants, while the combined supplementation barely affected gene expression, with VEHT showing a prooxidant/proinflamatory functional profile similar to C animals. Different hypothesis are proposed to explain this unexpected result. Findings allow a deeper understanding of the processes taking place in adipose tissue of genetically fat animals and the role of antioxidants in the regulation of fat cells function.

MeSH terms

  • Adipocytes / drug effects
  • Adipocytes / metabolism
  • Adipose Tissue* / drug effects
  • Adipose Tissue* / metabolism
  • Animal Feed / analysis
  • Animals
  • Antioxidants* / metabolism
  • Dietary Supplements*
  • Female
  • Maternal Nutritional Physiological Phenomena
  • Phenylethyl Alcohol* / administration & dosage
  • Phenylethyl Alcohol* / analogs & derivatives
  • Phenylethyl Alcohol* / pharmacology
  • Pregnancy
  • Swine
  • Transcriptome* / drug effects
  • Vitamin E / administration & dosage
  • Vitamin E / pharmacology
  • Weaning*

Substances

  • Antioxidants
  • Phenylethyl Alcohol
  • 3,4-dihydroxyphenylethanol
  • Vitamin E

Grants and funding

This work received grants PID2019-108695RB-C31 funded by MICIU/AEI/10.13039/501100011033/ and PID2022-139367OB-C21 funded by MICIU/AEI/10.13039/501100011033 and ERDF/EU. HDL received a grant from the Spanish Government: PRE2020-092891, funded by MICIU/AEI/10.13039/501100011033/ and by “ESF Investing in your future”; and GG received a grant from IRIAF-Sánchez Romero Carvajal Jabugo S.A. agreement. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.