Phospholipid peroxidation-driven modification of chondrogenic transcription factor mediates alkoxyl radicals-induced impairment of embryonic bone development
Maternal stress has been associated with poor birth outcomes, including preterm birth, infant mortality, and low birth weight. Bone development disorders in the embryo as a result of maternal stress are believed to be mediated through oxidative stress damage. Various species of free radicals, such a...
| Main Authors: | , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2022-10-01
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| Series: | Redox Biology |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213231722002099 |
| _version_ | 1811267013628133376 |
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| author | Jie Niu Xin Wan Gui-Yuan Yu Shan Jiang Ruo-Nan Yi Yan-Ping Wu Shu-Hua Ouyang Lei Liang Hiroshi Kurihara Wan-Yang Sun Xiao-Feng Zhu Rong-Hua Zhang Yun-Feng Cao Jian-Bo He Wen-Jun Duan Yi-Fang Li Rong-Rong He |
| author_facet | Jie Niu Xin Wan Gui-Yuan Yu Shan Jiang Ruo-Nan Yi Yan-Ping Wu Shu-Hua Ouyang Lei Liang Hiroshi Kurihara Wan-Yang Sun Xiao-Feng Zhu Rong-Hua Zhang Yun-Feng Cao Jian-Bo He Wen-Jun Duan Yi-Fang Li Rong-Rong He |
| author_sort | Jie Niu |
| collection | DOAJ |
| description | Maternal stress has been associated with poor birth outcomes, including preterm birth, infant mortality, and low birth weight. Bone development disorders in the embryo as a result of maternal stress are believed to be mediated through oxidative stress damage. Various species of free radicals, such as alkoxyl radicals, can be formed through endogenous redox response or exogenous stimuli in the womb and transmitted to embryos. Yet, whether these free radicals lead to abnormal fetal bone development is unclear. Here, we demonstrate prenatal bone growth retardation and ferroptosis-related signals of chondrocytes were induced by classic alkoxyl radical generators. We also show that alkoxyl radicals lead to significant accumulation of oxidized phospholipids in chondrocytes, through the iron-mediated Fenton reaction in embryos. We further demonstrate a role for the lipid peroxidation end product, 4-HNE, which forms adducts with the pivotal chondrogenesis transcription factor SOX9, leading to its degradation, therefore dampening chondrogenesis. Our data define a critical role for phospholipid peroxidation in alkoxyl radicals-evoked abnormal chondrogenesis, and pinpoint it being a precise target for treating oxidative stress-related bone development disorders. |
| first_indexed | 2024-04-12T20:53:37Z |
| format | Article |
| id | doaj.art-900e328e7e9c420a99557686efca05e2 |
| institution | Directory Open Access Journal |
| issn | 2213-2317 |
| language | English |
| last_indexed | 2024-04-12T20:53:37Z |
| publishDate | 2022-10-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Redox Biology |
| spelling | doaj.art-900e328e7e9c420a99557686efca05e22022-12-22T03:17:02ZengElsevierRedox Biology2213-23172022-10-0156102437Phospholipid peroxidation-driven modification of chondrogenic transcription factor mediates alkoxyl radicals-induced impairment of embryonic bone developmentJie Niu0Xin Wan1Gui-Yuan Yu2Shan Jiang3Ruo-Nan Yi4Yan-Ping Wu5Shu-Hua Ouyang6Lei Liang7Hiroshi Kurihara8Wan-Yang Sun9Xiao-Feng Zhu10Rong-Hua Zhang11Yun-Feng Cao12Jian-Bo He13Wen-Jun Duan14Yi-Fang Li15Rong-Rong He16Guangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China; International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Chinese Ministry of Education (MOE), Jinan University, Guangzhou, 510632, China; Guangdong Province Key Laboratory of Pharmacodynamic Constituents of TCM and New Drugs Research, Jinan University, Guangzhou, 510632, China; Joint Laboratory of Dalian Runsheng Kangtai and Jinan University, Jinan University, ChinaGuangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China; International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Chinese Ministry of Education (MOE), Jinan University, Guangzhou, 510632, China; Guangdong Province Key Laboratory of Pharmacodynamic Constituents of TCM and New Drugs Research, Jinan University, Guangzhou, 510632, China; Huizhou Health Sciences Polytechnic, Huizhou, 516025, ChinaGuangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China; International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Chinese Ministry of Education (MOE), Jinan University, Guangzhou, 510632, China; Guangdong Province Key Laboratory of Pharmacodynamic Constituents of TCM and New Drugs Research, Jinan University, Guangzhou, 510632, ChinaGuangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China; International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Chinese Ministry of Education (MOE), Jinan University, Guangzhou, 510632, China; Guangdong Province Key Laboratory of Pharmacodynamic Constituents of TCM and New Drugs Research, Jinan University, Guangzhou, 510632, China; Joint Laboratory of Dalian Runsheng Kangtai and Jinan University, Jinan University, ChinaGuangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China; International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Chinese Ministry of Education (MOE), Jinan University, Guangzhou, 510632, China; Guangdong Province Key Laboratory of Pharmacodynamic Constituents of TCM and New Drugs Research, Jinan University, Guangzhou, 510632, ChinaGuangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China; International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Chinese Ministry of Education (MOE), Jinan University, Guangzhou, 510632, China; Guangdong Province Key Laboratory of Pharmacodynamic Constituents of TCM and New Drugs Research, Jinan University, Guangzhou, 510632, China; Integrated Chinese and Western Medicine Department, School of Traditional Chinese Medicine, Jinan University, Guangzhou, 510632, China; Joint Laboratory of Dalian Runsheng Kangtai and Jinan University, Jinan University, ChinaGuangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China; International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Chinese Ministry of Education (MOE), Jinan University, Guangzhou, 510632, China; Guangdong Province Key Laboratory of Pharmacodynamic Constituents of TCM and New Drugs Research, Jinan University, Guangzhou, 510632, China; Integrated Chinese and Western Medicine Department, School of Traditional Chinese Medicine, Jinan University, Guangzhou, 510632, China; Joint Laboratory of Dalian Runsheng Kangtai and Jinan University, Jinan University, ChinaGuangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China; International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Chinese Ministry of Education (MOE), Jinan University, Guangzhou, 510632, China; Guangdong Province Key Laboratory of Pharmacodynamic Constituents of TCM and New Drugs Research, Jinan University, Guangzhou, 510632, China; Integrated Chinese and Western Medicine Department, School of Traditional Chinese Medicine, Jinan University, Guangzhou, 510632, China; Joint Laboratory of Dalian Runsheng Kangtai and Jinan University, Jinan University, ChinaGuangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China; International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Chinese Ministry of Education (MOE), Jinan University, Guangzhou, 510632, China; Guangdong Province Key Laboratory of Pharmacodynamic Constituents of TCM and New Drugs Research, Jinan University, Guangzhou, 510632, China; Joint Laboratory of Dalian Runsheng Kangtai and Jinan University, Jinan University, ChinaGuangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China; International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Chinese Ministry of Education (MOE), Jinan University, Guangzhou, 510632, China; Guangdong Province Key Laboratory of Pharmacodynamic Constituents of TCM and New Drugs Research, Jinan University, Guangzhou, 510632, China; Joint Laboratory of Dalian Runsheng Kangtai and Jinan University, Jinan University, ChinaGuangdong Provincial Key Laboratory of Traditional Chinese Medicine Informatization, Jinan University, Guangzhou, 510632, ChinaGuangdong Provincial Key Laboratory of Traditional Chinese Medicine Informatization, Jinan University, Guangzhou, 510632, ChinaJoint Laboratory of Dalian Runsheng Kangtai and Jinan University, Jinan University, China; Shanghai Institute for Biomedical and Pharmaceutical Technologies, NHC Key Laboratory of Reproduction Regulation, ShangHai 200032, ChinaGuangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China; International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Chinese Ministry of Education (MOE), Jinan University, Guangzhou, 510632, China; Guangdong Province Key Laboratory of Pharmacodynamic Constituents of TCM and New Drugs Research, Jinan University, Guangzhou, 510632, China; Integrated Chinese and Western Medicine Department, School of Traditional Chinese Medicine, Jinan University, Guangzhou, 510632, China; Joint Laboratory of Dalian Runsheng Kangtai and Jinan University, Jinan University, China; Corresponding author. Guangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China.Guangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China; International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Chinese Ministry of Education (MOE), Jinan University, Guangzhou, 510632, China; Guangdong Province Key Laboratory of Pharmacodynamic Constituents of TCM and New Drugs Research, Jinan University, Guangzhou, 510632, China; Integrated Chinese and Western Medicine Department, School of Traditional Chinese Medicine, Jinan University, Guangzhou, 510632, China; Joint Laboratory of Dalian Runsheng Kangtai and Jinan University, Jinan University, China; Corresponding author. Guangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China.Guangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China; International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Chinese Ministry of Education (MOE), Jinan University, Guangzhou, 510632, China; Guangdong Province Key Laboratory of Pharmacodynamic Constituents of TCM and New Drugs Research, Jinan University, Guangzhou, 510632, China; Joint Laboratory of Dalian Runsheng Kangtai and Jinan University, Jinan University, China; Corresponding author. Guangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China.Guangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China; International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Chinese Ministry of Education (MOE), Jinan University, Guangzhou, 510632, China; Guangdong Province Key Laboratory of Pharmacodynamic Constituents of TCM and New Drugs Research, Jinan University, Guangzhou, 510632, China; Integrated Chinese and Western Medicine Department, School of Traditional Chinese Medicine, Jinan University, Guangzhou, 510632, China; Joint Laboratory of Dalian Runsheng Kangtai and Jinan University, Jinan University, China; Corresponding author. Guangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility, Jinan University, Guangzhou, 510632, China.Maternal stress has been associated with poor birth outcomes, including preterm birth, infant mortality, and low birth weight. Bone development disorders in the embryo as a result of maternal stress are believed to be mediated through oxidative stress damage. Various species of free radicals, such as alkoxyl radicals, can be formed through endogenous redox response or exogenous stimuli in the womb and transmitted to embryos. Yet, whether these free radicals lead to abnormal fetal bone development is unclear. Here, we demonstrate prenatal bone growth retardation and ferroptosis-related signals of chondrocytes were induced by classic alkoxyl radical generators. We also show that alkoxyl radicals lead to significant accumulation of oxidized phospholipids in chondrocytes, through the iron-mediated Fenton reaction in embryos. We further demonstrate a role for the lipid peroxidation end product, 4-HNE, which forms adducts with the pivotal chondrogenesis transcription factor SOX9, leading to its degradation, therefore dampening chondrogenesis. Our data define a critical role for phospholipid peroxidation in alkoxyl radicals-evoked abnormal chondrogenesis, and pinpoint it being a precise target for treating oxidative stress-related bone development disorders.http://www.sciencedirect.com/science/article/pii/S2213231722002099Lipid peroxidationFerroptosisAlkoxyl radicalsChondrogenic transcription factorEmbryonic bone developmentChondrogenesis |
| spellingShingle | Jie Niu Xin Wan Gui-Yuan Yu Shan Jiang Ruo-Nan Yi Yan-Ping Wu Shu-Hua Ouyang Lei Liang Hiroshi Kurihara Wan-Yang Sun Xiao-Feng Zhu Rong-Hua Zhang Yun-Feng Cao Jian-Bo He Wen-Jun Duan Yi-Fang Li Rong-Rong He Phospholipid peroxidation-driven modification of chondrogenic transcription factor mediates alkoxyl radicals-induced impairment of embryonic bone development Redox Biology Lipid peroxidation Ferroptosis Alkoxyl radicals Chondrogenic transcription factor Embryonic bone development Chondrogenesis |
| title | Phospholipid peroxidation-driven modification of chondrogenic transcription factor mediates alkoxyl radicals-induced impairment of embryonic bone development |
| title_full | Phospholipid peroxidation-driven modification of chondrogenic transcription factor mediates alkoxyl radicals-induced impairment of embryonic bone development |
| title_fullStr | Phospholipid peroxidation-driven modification of chondrogenic transcription factor mediates alkoxyl radicals-induced impairment of embryonic bone development |
| title_full_unstemmed | Phospholipid peroxidation-driven modification of chondrogenic transcription factor mediates alkoxyl radicals-induced impairment of embryonic bone development |
| title_short | Phospholipid peroxidation-driven modification of chondrogenic transcription factor mediates alkoxyl radicals-induced impairment of embryonic bone development |
| title_sort | phospholipid peroxidation driven modification of chondrogenic transcription factor mediates alkoxyl radicals induced impairment of embryonic bone development |
| topic | Lipid peroxidation Ferroptosis Alkoxyl radicals Chondrogenic transcription factor Embryonic bone development Chondrogenesis |
| url | http://www.sciencedirect.com/science/article/pii/S2213231722002099 |
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