Maternal fish oil supplementation enhances placental nutrient transport and mammary gland secretion via the GPR120 signaling pathway

Qihui Li; Qianzi Zhang; Senlin Su; Siwang Yang; Jiayuan Shao; Wutai Guan; Shihai Zhang

doi:10.1016/j.jare.2024.12.029

Maternal fish oil supplementation enhances placental nutrient transport and mammary gland secretion via the GPR120 signaling pathway

J Adv Res. 2024 Dec 18:S2090-1232(24)00607-6. doi: 10.1016/j.jare.2024.12.029. Online ahead of print.

Authors

Qihui Li¹, Qianzi Zhang², Senlin Su², Siwang Yang², Jiayuan Shao², Wutai Guan³, Shihai Zhang⁴

Affiliations

¹ Guangdong Province Key Laboratory of Animal Nutrition Control, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. Electronic address: 3407lqh@stu.scau.edu.cn.
² Guangdong Province Key Laboratory of Animal Nutrition Control, College of Animal Science, South China Agricultural University, Guangzhou 510642, China.
³ Guangdong Province Key Laboratory of Animal Nutrition Control, College of Animal Science, South China Agricultural University, Guangzhou 510642, China; College of Animal Science and National Engineering Research Center for Breeding Swine Industry, South China Agricultural University, Guangzhou 510642, China; Guangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou 510642, China.
⁴ Guangdong Province Key Laboratory of Animal Nutrition Control, College of Animal Science, South China Agricultural University, Guangzhou 510642, China; College of Animal Science and National Engineering Research Center for Breeding Swine Industry, South China Agricultural University, Guangzhou 510642, China; Guangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou 510642, China. Electronic address: zhangshihai@scau.edu.cn.

PMID: 39706333
DOI: 10.1016/j.jare.2024.12.029

Abstract

Introduction: Maternal fish oil (FO) supplementation during pregnancy has been shown to improve pregnancy outcomes. FO is recognized as dietary source for n-3 polyunsaturated fatty acids (n-3 PUFAs). While early research has focused on the benefits of n-3 polyunsaturated fatty acids n-3 PUFAs for fetal neurodevelopment, retinal maturation and neonatal behavior, their roles in the placenta during late pregnancy and in the mammary gland during lactation still remain unknow.

Objectives: Here, we aim to clarify the mechanisms by which maternal supplementation with FO during pregnancy and lactation affects placental and mammary gland function.

Methods: We evaluated the effects of FO on maternal placental nutrient transport, mammary gland milk synthesis and offspring growth. We then explored the molecular mechanisms by which docosahexaenoic acid (DHA) affects the function of placental trophoblast cells and nutrient secretion of mammary epithelial cells through in vitro experiments. Finally, a lipopolysaccharide-challenged experiment was performed to access the potential of maternal FO supplementation in alleviating offspring intestinal inflammation.

Results: Maternal supplementation with FO during late pregnancy increased offspring birth weight, associated with enhanced maternal placental vascularization and nutrient transporter abundance. Additionally, maternal FO supplementation during lactation improved mammary gland secretion, increasing the fat, protein, and non-fat solids content in both colostrum and mature milk, thereby promoting offspring growth. The stimulatory effects of DHA on placental trophoblast cell function and nutrient secretion in mammary gland epithelial cells were mediated by GPR120 signaling pathways. Furthermore, maternal FO supplementation strengthened the placental barrier, reduced placental inflammation, oxidative stress and alleviated lipopolysaccharide-induced intestinal inflammation in offspring.

Conclusion: Maternal FO supplementation during late pregnancy and lactation enhances offspring growth by increasing placental nutrient transport and mammary gland secretion function, mediated by GPR120. Additionally, maternal FO supplementation reduces the susceptibility of offspring to intestinal inflammation.

Keywords: Fish oil; GPR120; Mammary gland; N-3 polyunsaturated fatty acids; Placenta.