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Inhibition of Maternal c-Src Ameliorates the Male Offspring Hypertension by Suppressing Inflammation and Neurotransmitters in the Paraventricular Nucleus

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Abstract

Long-term maternal salt intake induces the hypertension in offspring. Numerous studies have also indicated that high-salt diet causes the inflammation and an imbalance in neurotransmitters in the paraventricular nucleus (PVN) which increases the blood pressure and sympathetic activity. This study aimed to explore whether maternal salt intake induces hypertension in their male offspring by increasing the inflammation and changing the neurotransmitters balance in the paraventricular nucleus of offspring. This study includes two parts: Part I to explore the effect of high-salt diet on pregnant rats and the changes in inflammation and neurotransmitters in their male offspring PVN; Part II to reveal the influence on their offspring of bilateral PVN infusion of c-Src inhibitor dasatinib (DAS) in pregnant rats fed a high-salt diet. Maternal high-salt diet intake during copulation, pregnancy, and lactation impacted the offspring mean arterial pressure (MAP) and elevated the offspring PVN levels of p-Src, proinflammatory cytokines, and excitatory neurotransmitters. Bilateral PVN infusion of a c-Src inhibitor combined with maternal high-salt diets decreased MAP in the offspring. The infusion was also shown to suppress the Src-induced MAPK/NF-κB signaling pathway (p38 MAPK, JNK, Erk1/2), which attenuates inflammatory reactions. Finally, bilateral PVN infusion of the Src inhibitor in pregnant rat with high-salt diets improved the levels of inhibitory neurotransmitters in offspring PVN, which restored the excitatory-inhibitory neurotransmitter balance in male offspring. High-salt diets increase sympathetic activity and blood pressure in adult offspring, probably by activating the c-Src/MAPKs/NF-κB signaling pathway-induced inflammation. Moreover, NF-κB disrupts the downstream excitatory-inhibitory neurotransmitter balance in the PVN of male offspring.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 81800373, 82070439, 81770426, 81700373, 82070440), Shaanxi Basic Research on Natural Science (Nos. 2019JQ-263, 2020JM-079), the China Postdoctoral Science Foundation (No. 2019M660259).

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  1. Qing Su and Xiao-Jing Yu are these authors contributed equally to this study.

Authors and Affiliations

  1. Department of Physiology and Pathophysiology, Shaanxi Engineering and Research Center of Vaccine, Key Laboratory of Environment and Genes Related to Diseases of Education Ministry of China, Xi’an Jiaotong University School of Basic Medical Sciences, Xi’an, 710061, China

    Qing Su, Xiao-Jing Yu, Xiao-Min Wang, Wen-Jie Xia, Hong-Bao Li, Kai-Li Liu & Yu-Ming Kang

  2. School of Sport and Health Sciences, Xi’an Physical Education University, Xi’an, 710068, China

    Qing Yang

  3. Clinical Pharmacological Institution, The First Affiliated Hospital of Xi’an Jiaotong University, Xi’an, 710061, China

    Qiu-Yue Yi

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Contributions

QS, XJY, and YMK designed the study. QS, QY, HBL, and WJX performed all experiments. QY, HBL, XMW, XJY, and QS also performed, checked the data analysis, and drafted the manuscript. QY, XMW, and KLL participated in data analysis. XMW helped to check the responses and revised manuscript. All authors reviewed the final manuscript.

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Correspondence to Xiao-Jing Yu or Yu-Ming Kang.

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Su, Q., Yu, XJ., Yang, Q. et al. Inhibition of Maternal c-Src Ameliorates the Male Offspring Hypertension by Suppressing Inflammation and Neurotransmitters in the Paraventricular Nucleus. Cardiovasc Toxicol 21, 820–834 (2021). https://doi.org/10.1007/s12012-021-09672-z

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