The imprinted Igf2-Igf2r axis is critical for exosome biogenesis during the early development of bovine placenta

Insulin-like growth factor 2 (IGF2) is essential for cell growth and differentiation and functions through the IGF2 receptor (IGF2R) to regulate embryonic and placental development. Exosomes that are synthesized and released from cells and play important roles in embryogenesis and placental developm...

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Main Authors: Kunhua ZHENG, Longfei XIAO, Naihan YUAN, Xihui SHENG, Xiaolong QI, Yingqiu WANG, Chang CHEN, Kaijun GUO, Lin YANG, Bingying LIU, Xiangguo WANG
Format: Article
Language:English
Published: The Society for Reproduction and Development 2024-12-01
Series:The Journal of Reproduction and Development
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Online Access:https://www.jstage.jst.go.jp/article/jrd/71/1/71_2024-081/_pdf/-char/en
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author Kunhua ZHENG
Longfei XIAO
Naihan YUAN
Xihui SHENG
Xiaolong QI
Yingqiu WANG
Chang CHEN
Kaijun GUO
Lin YANG
Bingying LIU
Xiangguo WANG
author_facet Kunhua ZHENG
Longfei XIAO
Naihan YUAN
Xihui SHENG
Xiaolong QI
Yingqiu WANG
Chang CHEN
Kaijun GUO
Lin YANG
Bingying LIU
Xiangguo WANG
author_sort Kunhua ZHENG
collection DOAJ
description Insulin-like growth factor 2 (IGF2) is essential for cell growth and differentiation and functions through the IGF2 receptor (IGF2R) to regulate embryonic and placental development. Exosomes that are synthesized and released from cells and play important roles in embryogenesis and placental development rely on the IGF2R for sorting and transport. However, the role of the imprinted Igf2-Igr2r axis and exosomes in the co-regulation of early placental development remains unknown. Cotyledon villi were collected from bovine placentas at different gestational ages, and the localization and expression of IGF2, IGF2R, and exosomal marker proteins were detected. Furthermore, the expression of exosomal marker factors was detected after the expression of IGF2R or IGF2 was inhibited through RNA interference or the addition of inhibitors, respectively. Our results demonstrated that IGF2, IGF2R, and the exosomal markers CD63, CD9, TSG101, and Rab11 are mainly located on the cell membrane of mononuclear trophoblast cells and binuclear trophoblast cells, which make up the cotyledon villi of the bovine placenta. The expressions of IGF2, IGF2R, and the exosomal marker proteins CD63, CD9, TSG101, and Rab11 showed a significant upward trend with increased gestation duration. Additionally, both Igf2r-knockdown and suppressing the expression of IGF2 with chromeceptin (IGF2 inhibitor) led to the downregulation of exosomal marker proteins in both bovine placental trophoblast cells (BTCs) and BTC-derived exosomes. Our study confirmed that the imprinted Igf2-Igf2r axis participates in the early development of cotyledon villi in the bovine placenta by manipulating exosome biogenesis, providing evidence for improving disorders during placental development.
format Article
id doaj-art-5195cfa61c5b45d399ed47c06fbba5ad
institution Kabale University
issn 0916-8818
1348-4400
language English
publishDate 2024-12-01
publisher The Society for Reproduction and Development
record_format Article
series The Journal of Reproduction and Development
spelling doaj-art-5195cfa61c5b45d399ed47c06fbba5ad2025-02-04T23:41:35ZengThe Society for Reproduction and DevelopmentThe Journal of Reproduction and Development0916-88181348-44002024-12-01711414810.1262/jrd.2024-081jrdThe imprinted Igf2-Igf2r axis is critical for exosome biogenesis during the early development of bovine placentaKunhua ZHENG0Longfei XIAO1Naihan YUAN2Xihui SHENG3Xiaolong QI4Yingqiu WANG5Chang CHEN6Kaijun GUO7Lin YANG8Bingying LIU9Xiangguo WANG10Animal Science and Technology College, Beijing University of Agriculture, Beijing 102206, ChinaAnimal Science and Technology College, Beijing University of Agriculture, Beijing 102206, ChinaAnimal Science and Technology College, Beijing University of Agriculture, Beijing 102206, ChinaAnimal Science and Technology College, Beijing University of Agriculture, Beijing 102206, ChinaAnimal Science and Technology College, Beijing University of Agriculture, Beijing 102206, ChinaAnimal Science and Technology College, Beijing University of Agriculture, Beijing 102206, ChinaAnimal Science and Technology College, Beijing University of Agriculture, Beijing 102206, ChinaAnimal Science and Technology College, Beijing University of Agriculture, Beijing 102206, ChinaAnimal Epidemic prevention and Quarantine center, Huimin District, Inner Mongolia Autonomous Region 010030, ChinaAnimal Science and Technology College, Beijing University of Agriculture, Beijing 102206, ChinaAnimal Science and Technology College, Beijing University of Agriculture, Beijing 102206, ChinaInsulin-like growth factor 2 (IGF2) is essential for cell growth and differentiation and functions through the IGF2 receptor (IGF2R) to regulate embryonic and placental development. Exosomes that are synthesized and released from cells and play important roles in embryogenesis and placental development rely on the IGF2R for sorting and transport. However, the role of the imprinted Igf2-Igr2r axis and exosomes in the co-regulation of early placental development remains unknown. Cotyledon villi were collected from bovine placentas at different gestational ages, and the localization and expression of IGF2, IGF2R, and exosomal marker proteins were detected. Furthermore, the expression of exosomal marker factors was detected after the expression of IGF2R or IGF2 was inhibited through RNA interference or the addition of inhibitors, respectively. Our results demonstrated that IGF2, IGF2R, and the exosomal markers CD63, CD9, TSG101, and Rab11 are mainly located on the cell membrane of mononuclear trophoblast cells and binuclear trophoblast cells, which make up the cotyledon villi of the bovine placenta. The expressions of IGF2, IGF2R, and the exosomal marker proteins CD63, CD9, TSG101, and Rab11 showed a significant upward trend with increased gestation duration. Additionally, both Igf2r-knockdown and suppressing the expression of IGF2 with chromeceptin (IGF2 inhibitor) led to the downregulation of exosomal marker proteins in both bovine placental trophoblast cells (BTCs) and BTC-derived exosomes. Our study confirmed that the imprinted Igf2-Igf2r axis participates in the early development of cotyledon villi in the bovine placenta by manipulating exosome biogenesis, providing evidence for improving disorders during placental development.https://www.jstage.jst.go.jp/article/jrd/71/1/71_2024-081/_pdf/-char/enbovineexosomesinsulin-like growth factor 2 (igf2)insulin-like growth factor 2 receptor (igf2r)placental trophoblast cells
spellingShingle Kunhua ZHENG
Longfei XIAO
Naihan YUAN
Xihui SHENG
Xiaolong QI
Yingqiu WANG
Chang CHEN
Kaijun GUO
Lin YANG
Bingying LIU
Xiangguo WANG
The imprinted Igf2-Igf2r axis is critical for exosome biogenesis during the early development of bovine placenta
The Journal of Reproduction and Development
bovine
exosomes
insulin-like growth factor 2 (igf2)
insulin-like growth factor 2 receptor (igf2r)
placental trophoblast cells
title The imprinted Igf2-Igf2r axis is critical for exosome biogenesis during the early development of bovine placenta
title_full The imprinted Igf2-Igf2r axis is critical for exosome biogenesis during the early development of bovine placenta
title_fullStr The imprinted Igf2-Igf2r axis is critical for exosome biogenesis during the early development of bovine placenta
title_full_unstemmed The imprinted Igf2-Igf2r axis is critical for exosome biogenesis during the early development of bovine placenta
title_short The imprinted Igf2-Igf2r axis is critical for exosome biogenesis during the early development of bovine placenta
title_sort imprinted igf2 igf2r axis is critical for exosome biogenesis during the early development of bovine placenta
topic bovine
exosomes
insulin-like growth factor 2 (igf2)
insulin-like growth factor 2 receptor (igf2r)
placental trophoblast cells
url https://www.jstage.jst.go.jp/article/jrd/71/1/71_2024-081/_pdf/-char/en
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