2-bromoacetamide exposure impairs oocyte maturation in mice and humans primarily via disrupting the cytoskeleton

Chuanxin Zhang; Xiaoyu Yin; Xueqi Dong; Mingze Shi; Yuxin Xu; Jiayin Gao; Jiawei Wang; Jinzhu Song; Boyang Liu; Keliang Wu

Ecotoxicology and Environmental Safety (Mar 2024)

2-bromoacetamide exposure impairs oocyte maturation in mice and humans primarily via disrupting the cytoskeleton

Chuanxin Zhang,
Xiaoyu Yin,
Xueqi Dong,
Mingze Shi,
Yuxin Xu,
Jiayin Gao,
Jiawei Wang,
Jinzhu Song,
Boyang Liu,
Keliang Wu

Affiliations

Chuanxin Zhang: Center for Reproductive Medicine, Shandong University, Jinan, Shandong 250012, China; Key Laboratory of Reproductive Endocrinology of Ministry of Education, Shandong University, Jinan, Shandong 250012, China; Shandong Key Laboratory of Reproductive Medicine, Jinan, Shandong 250012, China; Shandong Provincial Clinical Research Center for Reproductive Health, Jinan, Shandong 250012, China; Shandong Technology Innovation Center for Reproductive Health, Jinan, Shandong 250012, China; National Research Center for Assisted Reproductive Technology and Reproductive Genetics, Shandong University, Jinan, Shandong 250012, China; State Key Laboratory of Reproductive Medicine and Offspring Health, Shandong University, Jinan, Shandong 250012, China
Xiaoyu Yin: Center for Reproductive Medicine, Shandong University, Jinan, Shandong 250012, China; Key Laboratory of Reproductive Endocrinology of Ministry of Education, Shandong University, Jinan, Shandong 250012, China; Shandong Key Laboratory of Reproductive Medicine, Jinan, Shandong 250012, China; Shandong Provincial Clinical Research Center for Reproductive Health, Jinan, Shandong 250012, China; Shandong Technology Innovation Center for Reproductive Health, Jinan, Shandong 250012, China; National Research Center for Assisted Reproductive Technology and Reproductive Genetics, Shandong University, Jinan, Shandong 250012, China; State Key Laboratory of Reproductive Medicine and Offspring Health, Shandong University, Jinan, Shandong 250012, China
Xueqi Dong: Center for Reproductive Medicine, Shandong University, Jinan, Shandong 250012, China; Key Laboratory of Reproductive Endocrinology of Ministry of Education, Shandong University, Jinan, Shandong 250012, China; Shandong Key Laboratory of Reproductive Medicine, Jinan, Shandong 250012, China; Shandong Provincial Clinical Research Center for Reproductive Health, Jinan, Shandong 250012, China; Shandong Technology Innovation Center for Reproductive Health, Jinan, Shandong 250012, China; National Research Center for Assisted Reproductive Technology and Reproductive Genetics, Shandong University, Jinan, Shandong 250012, China; State Key Laboratory of Reproductive Medicine and Offspring Health, Shandong University, Jinan, Shandong 250012, China
Mingze Shi: Center for Reproductive Medicine, Shandong University, Jinan, Shandong 250012, China; Key Laboratory of Reproductive Endocrinology of Ministry of Education, Shandong University, Jinan, Shandong 250012, China; Shandong Key Laboratory of Reproductive Medicine, Jinan, Shandong 250012, China; Shandong Provincial Clinical Research Center for Reproductive Health, Jinan, Shandong 250012, China; Shandong Technology Innovation Center for Reproductive Health, Jinan, Shandong 250012, China; National Research Center for Assisted Reproductive Technology and Reproductive Genetics, Shandong University, Jinan, Shandong 250012, China; State Key Laboratory of Reproductive Medicine and Offspring Health, Shandong University, Jinan, Shandong 250012, China
Yuxin Xu: Center for Reproductive Medicine, Shandong University, Jinan, Shandong 250012, China; Key Laboratory of Reproductive Endocrinology of Ministry of Education, Shandong University, Jinan, Shandong 250012, China; Shandong Key Laboratory of Reproductive Medicine, Jinan, Shandong 250012, China; Shandong Provincial Clinical Research Center for Reproductive Health, Jinan, Shandong 250012, China; Shandong Technology Innovation Center for Reproductive Health, Jinan, Shandong 250012, China; National Research Center for Assisted Reproductive Technology and Reproductive Genetics, Shandong University, Jinan, Shandong 250012, China; State Key Laboratory of Reproductive Medicine and Offspring Health, Shandong University, Jinan, Shandong 250012, China
Jiayin Gao: Center for Reproductive Medicine, Shandong University, Jinan, Shandong 250012, China; Key Laboratory of Reproductive Endocrinology of Ministry of Education, Shandong University, Jinan, Shandong 250012, China; Shandong Key Laboratory of Reproductive Medicine, Jinan, Shandong 250012, China; Shandong Provincial Clinical Research Center for Reproductive Health, Jinan, Shandong 250012, China; Shandong Technology Innovation Center for Reproductive Health, Jinan, Shandong 250012, China; National Research Center for Assisted Reproductive Technology and Reproductive Genetics, Shandong University, Jinan, Shandong 250012, China; State Key Laboratory of Reproductive Medicine and Offspring Health, Shandong University, Jinan, Shandong 250012, China
Jiawei Wang: Center for Reproductive Medicine, Shandong University, Jinan, Shandong 250012, China; Key Laboratory of Reproductive Endocrinology of Ministry of Education, Shandong University, Jinan, Shandong 250012, China; Shandong Key Laboratory of Reproductive Medicine, Jinan, Shandong 250012, China; Shandong Provincial Clinical Research Center for Reproductive Health, Jinan, Shandong 250012, China; Shandong Technology Innovation Center for Reproductive Health, Jinan, Shandong 250012, China; National Research Center for Assisted Reproductive Technology and Reproductive Genetics, Shandong University, Jinan, Shandong 250012, China; State Key Laboratory of Reproductive Medicine and Offspring Health, Shandong University, Jinan, Shandong 250012, China
Jinzhu Song: Center for Reproductive Medicine, Shandong University, Jinan, Shandong 250012, China; Key Laboratory of Reproductive Endocrinology of Ministry of Education, Shandong University, Jinan, Shandong 250012, China; Shandong Key Laboratory of Reproductive Medicine, Jinan, Shandong 250012, China; Shandong Provincial Clinical Research Center for Reproductive Health, Jinan, Shandong 250012, China; Shandong Technology Innovation Center for Reproductive Health, Jinan, Shandong 250012, China; National Research Center for Assisted Reproductive Technology and Reproductive Genetics, Shandong University, Jinan, Shandong 250012, China; State Key Laboratory of Reproductive Medicine and Offspring Health, Shandong University, Jinan, Shandong 250012, China
Boyang Liu: Center for Reproductive Medicine, Shandong University, Jinan, Shandong 250012, China; Key Laboratory of Reproductive Endocrinology of Ministry of Education, Shandong University, Jinan, Shandong 250012, China; Shandong Key Laboratory of Reproductive Medicine, Jinan, Shandong 250012, China; Shandong Provincial Clinical Research Center for Reproductive Health, Jinan, Shandong 250012, China; Shandong Technology Innovation Center for Reproductive Health, Jinan, Shandong 250012, China; National Research Center for Assisted Reproductive Technology and Reproductive Genetics, Shandong University, Jinan, Shandong 250012, China; State Key Laboratory of Reproductive Medicine and Offspring Health, Shandong University, Jinan, Shandong 250012, China
Keliang Wu: Center for Reproductive Medicine, Shandong University, Jinan, Shandong 250012, China; Key Laboratory of Reproductive Endocrinology of Ministry of Education, Shandong University, Jinan, Shandong 250012, China; Shandong Key Laboratory of Reproductive Medicine, Jinan, Shandong 250012, China; Shandong Provincial Clinical Research Center for Reproductive Health, Jinan, Shandong 250012, China; Shandong Technology Innovation Center for Reproductive Health, Jinan, Shandong 250012, China; National Research Center for Assisted Reproductive Technology and Reproductive Genetics, Shandong University, Jinan, Shandong 250012, China; State Key Laboratory of Reproductive Medicine and Offspring Health, Shandong University, Jinan, Shandong 250012, China; Correspondence to: Center for Reproductive Medicine, Shandong University, 157 Jingliu Road, Jinan 250021, China.

Journal volume & issue: Vol. 272
p. 116105

Abstract

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2-bromoacetamide (BAcAm) is an emerging class of unregulated disinfection by-products (DBPs), with potent cytogenetic and developmental toxicity in animals. However, whether BAcAm exerts toxic effects on mammalian oocyte quality remains to be elucidate. In this research, we investigated the effect of BAcAm on mouse and human oocyte maturation with an in vitro culture system. Our results revealed that BAcAm exposure hindered the extrusion of the first polar body, disrupted the spindle organization and reduced the competence of embryo development after fertilization in the mouse oocytes. Results of single-cell RNA sequencing (scRNA-seq) showed that 605 differentially expressed genes (DEGs) were identified in the BAcAm exposed mouse oocytes, among which 366 were up-regulated and 239 were down-regulated. Gene Ontology (GO) analysis further revealed that DEGs were mainly enriched in mitochondrial functions, oxidative stress, cytoskeleton, endoplasmic reticulum (ER), Golgi and protein synthesis, DNA damage and apoptosis. We then conducted further tests in these aspects and discovered that BAcAm exposure principally perturbed the function of microtubule and actin cytoskeleton. This finding was confirmed in human oocytes. Overall, our data suggest that BAcAm exposure disturbs the cytoskeleton function, thus impairing oocyte maturation. These data, for the first time, provide a comprehensive view for the toxic effects of BAcAm on oocyte maturation.

Published in Ecotoxicology and Environmental Safety

ISSN: 0147-6513 (Print); 1090-2414 (Online)
Publisher: Elsevier
Country of publisher: United States
LCC subjects: Technology: Environmental technology. Sanitary engineering: Environmental pollution; Geography. Anthropology. Recreation: Environmental sciences
Website: https://www.journals.elsevier.com/ecotoxicology-and-environmental-safety

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