Luteolin regulates the distribution and function of organelles by controlling SIRT1 activity during postovulatory oocyte aging

Xupeng Xing; Jingfeng Peng; Jingyu Zhao; Ruoxi Shi; Caiqin Wang; Zihan Zhang; Zihan Wang; Zicong Li; Zhenfang Wu

doi:10.3389/fnut.2023.1192758

Luteolin regulates the distribution and function of organelles by controlling SIRT1 activity during postovulatory oocyte aging

Front Nutr. 2023 Jul 31:10:1192758. doi: 10.3389/fnut.2023.1192758. eCollection 2023.

Authors

Xupeng Xing^{1

2}, Jingfeng Peng^{1

2}, Jingyu Zhao^{3

4}, Ruoxi Shi^{3

4}, Caiqin Wang^{3

4}, Zihan Zhang^{3

4}, Zihan Wang^{3

4}, Zicong Li^{1

2}, Zhenfang Wu^{1

2}

Affiliations

¹ National Engineering Research Center for Breeding Swine Industry, South China Agricultural University, Guangzhou, China.
² Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou, China.
³ Collaborative Innovation Center for Birth Defect Research and Transformation of Shandong Province, Jining Medical University, Jining, China.
⁴ College of Second Clinical Medical, Jining Medical University, Jining, China.

Abstract

The quality of oocytes determines their development competence, which will be rapidly lost if the oocytes are not fertilized at the proper time after ovulation. SIRT1, one of the sirtuin family members, has been proven to protect the quality of oocytes during postovulatory oocyte aging. However, evidence of the effect of SIRT1 on the activity of organelles including the mitochondria, the endoplasmic reticulum (ER), the Golgi apparatus, and the lysosomes in postovulatory aging oocyte is lacking. In this study, we investigated the distribution and function of organelles in postovulatory aged oocytes and discovered abnormalities. Luteolin, which is a natural flavonoid contained in vegetables and fruits, is an activator of SIRT1. When the oocytes were treated with luteolin, the abnormal distribution of mitochondria, ER, and Golgi complex were restored during postovulatory oocyte aging. The ER stress protein GRP78 and the lysosome protein LAMP1 increased, while the mitochondrial membrane potential and the Golgi complex protein GOLPH3 decreased in aged oocytes, and these were restored by luteolin treatment. EX-527, an inhibitor of SIRT1, disrupted the luteolin-mediated normal distribution and function of mitochondria, ER, Golgi apparatus, and lysosomes. In conclusion, we demonstrate that luteolin regulates the distribution and function of mitochondria, ER, Golgi apparatus, and lysosomes during postovulatory oocyte aging by activating SIRT1.

Keywords: SIRT1; aging-induced changes; luteolin; organelles; postovulatory oocyte aging.