Developmental competence of bovine early embryos depends on the coupled response between oxidative and endoplasmic reticulum stress.
The stress produced by the coupling of reactive oxygen species (ROS) and endoplasmic reticulum (ER) has been explored extensively, but little is known regarding their roles in the early development of mammalian embryos. Here, we demonstrated that the early development of in vitro-produced (IVP) bovine embryos was governed by the cooperative action between ROS and ER stress. Compared with the tension produced by 5% O2, 20% O2 significantly decreased the blastocyst formation rate and cell survival, which was accompanied by increases in ROS and in levels of sXBP-1 transcript, which is an ER stress indicator. In addition, treatment with glutathione (GSH), a ROS scavenger, decreased ROS levels, which resulted in increased blastocyst formation and cell survival rates. Importantly, levels of sXBP-1 and ER stress-associated transcripts were reduced by GSH treatment in developing bovine embryos. Consistent with this observation, tauroursodeoxycholate (TUDCA), an ER stress inhibitor, improved blastocyst developmental rate, trophectoderm proportion, and cell survival. Moreover, ROS and sXBP-1 transcript levels were markedly decreased by supplementation with TUDCA, suggesting a possible mechanism governing the mutual regulation between ROS and ER stress. Interestingly, knockdown of XBP-1 transcripts resulted in both elevation of ROS and decrease of antioxidant transcripts, which ultimately reduced in vitro developmental competence of bovine embryos. Based on these results, in vitro developmental competence of IVP bovine embryos was highly dependent on the coupled response between oxidative and ER stresses. These results increase our understanding of the mechanism(s) governing early embryonic development and may improve strategies for the generation of IVP embryos with high developmental competence.
National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea Department of Functional Genomics, University of Science and Technology, Daejeon, Republic of Korea.
Seung-Bin
SB
Yoon
National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea.
Seon-A
SA
Choi
National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea.
Bo-Woong
BW
Sim
National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea.
Ji-Su
JS
Kim
National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea.
Seong-Eun
SE
Mun
National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea.
Pil-Soo
PS
Jeong
National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea.
Hae-Jun
HJ
Yang
National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea.
Youngjeon
Y
Lee
National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea.
Young-Ho
YH
Park
National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea.
Bong-Seok
BS
Song
National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea.
Young-Hyun
YH
Kim
National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea.
Kang-Jin
KJ
Jeong
National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea Department of Functional Genomics, University of Science and Technology, Daejeon, Republic of Korea.
Jae-Won
JW
Huh
National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea Department of Functional Genomics, University of Science and Technology, Daejeon, Republic of Korea.
Sang-Rae
SR
Lee
National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea Department of Functional Genomics, University of Science and Technology, Daejeon, Republic of Korea sunuk@kribb.re.kr.
Sun-Uk
SU
Kim
National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea Department of Functional Genomics, University of Science and Technology, Daejeon, Republic of Korea changkt@kribb.re.kr.
Kyu-Tae
KT
Chang
D000818:Animals; D017209:Apoptosis / Q000502:physiology*; D015153:Blotting, Western / Q000662:veterinary; D002417:Cattle / Q000196:embryology*; D004622:Embryo, Mammalian / Q000502:physiology*; D047108:Embryonic Development / Q000502:physiology*; D059865:Endoplasmic Reticulum Stress / Q000502:physiology*; D005260:Female; D005978:Glutathione / Q000494:pharmacology; D020287:In Situ Nick-End Labeling / Q000662:veterinary; D008856:Microscopy, Fluorescence / Q000662:veterinary; D011247:Pregnancy; D034741:RNA, Small Interfering / Q000494:pharmacology; D017382:Reactive Oxygen Species / Q000378:metabolism; D013657:Taurodeoxycholic Acid / Q000494:pharmacology
D034741:RNA, Small Interfering; D017382:Reactive Oxygen Species; D013657:Taurodeoxycholic Acid; D005978:Glutathione
early development; embryo culture; endoplasmic reticulum stress; reactive oxygen species