Single-embryo transcriptomic atlas of oxygen response reveals the critical role of HIF-1α in prompting embryonic zygotic genome activation

Fusheng Yao; Meiqiang Chu; Guangyin Xi; Jiage Dai; Zhaochen Wang; Jia Hao; Qianying Yang; Wenjing Wang; Yawen Tang; Jingyu Zhang; Yuan Yue; Yue Wang; Yefen Xu; Wei Zhao; Lizhu Ma; Juan Liu; Zhenni Zhang; Jianhui Tian; Lei An

Redox Biology (Jun 2024)

Single-embryo transcriptomic atlas of oxygen response reveals the critical role of HIF-1α in prompting embryonic zygotic genome activation

Fusheng Yao,
Meiqiang Chu,
Guangyin Xi,
Jiage Dai,
Zhaochen Wang,
Jia Hao,
Qianying Yang,
Wenjing Wang,
Yawen Tang,
Jingyu Zhang,
Yuan Yue,
Yue Wang,
Yefen Xu,
Wei Zhao,
Lizhu Ma,
Juan Liu,
Zhenni Zhang,
Jianhui Tian,
Lei An

Affiliations

Fusheng Yao: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China
Meiqiang Chu: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China
Guangyin Xi: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China
Jiage Dai: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China
Zhaochen Wang: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China
Jia Hao: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China
Qianying Yang: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China
Wenjing Wang: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China
Yawen Tang: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China
Jingyu Zhang: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China
Yuan Yue: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China
Yue Wang: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China
Yefen Xu: Animal Science Department, Tibet Agricultural and Animal Husbandry College, 100 Yucai Road, Bayi District, Tibet, 860000, Nyingchi, PR China
Wei Zhao: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China
Lizhu Ma: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China
Juan Liu: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China
Zhenni Zhang: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China
Jianhui Tian: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China; Corresponding authors.
Lei An: National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No.2 Yuanmingyuan West Road, Beijing, 100193, PR China; Corresponding authors.

Journal volume & issue: Vol. 72
p. 103147

Abstract

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Adaptive response to physiological oxygen levels (physO2; 5% O2) enables embryonic survival in a low-oxygen developmental environment. However, the mechanism underlying the role of physO2 in supporting preimplantation development, remains elusive. Here, we systematically studied oxygen responses of hallmark events in preimplantation development. Focusing on impeded transcriptional upregulation under atmospheric oxygen levels (atmosO2; 20% O2) during the 2-cell stage, we functionally identified a novel role of HIF-1α in promoting major zygotic genome activation by serving as an oxygen-sensitive transcription factor. Moreover, during blastocyst formation, atmosO2 impeded H3K4me3 and H3K27me3 deposition by deregulating histone-lysine methyltransferases, thus impairing X-chromosome inactivation in blastocysts. In addition, we found atmosO2 impedes metabolic shift to glycolysis before blastocyst formation, thus resulting a low-level histone lactylation deposition. Notably, we also reported an increased sex-dimorphic oxygen response of embryos upon preimplantation development. Together, focusing on genetic and epigenetic events that are essential for embryonic survival and development, the present study advances current knowledge of embryonic adaptive responses to physO2, and provides novel insight into mechanism underlying irreversibly impaired developmental potential due to a short-term atmosO2 exposure.

Published in Redox Biology

ISSN: 2213-2317 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Medicine: Medicine (General); Science: Biology (General)
Website: http://www.journals.elsevier.com/redox-biology/

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